Protocorms and protocorm-like bodies are molecularly ... · 171 important/required for general and tissue-specific proliferation and maintenance of 172 meristematic tissues, a reference

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Protocorms and protocorm-like bodies are molecularly distinct from zygotic 1 embryonic tissues in Phalaenopsis aphrodite 2 Su-Chiung Fang1,2*, Jhun-Chen Chen1,2, Miao-Ju Wei1,2 3 4 1Biotechnology Center in Southern Taiwan, Academia Sinica, Tainan, 741, Taiwan 5 2Agricultural Biotechnology Research Center, Academia Sinica, Taipei, 115, Taiwan 6 7 8 9 Corresponding author: 10 Su-Chiung Fang 11 E-mail address: [email protected] 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29

Plant Physiology Preview. Published on June 23, 2016, as DOI:10.1104/pp.16.00841

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30 One sentence summary: 31 Protocorm-like-body (PLB) development does not utilize the somatic 32 embryogenesis program in Phalaenopsis aphrodite 33 34 35 36 37 Financial source: 38 This work was supported by the Development Program of Industrialization for 39 Agricultural Biotechnology grants (to SCF); and in part by a grant (to SCF) from the 40 Biotechnology Center in Southern Taiwan, Academia Sinica. 41 42 43 44 Author Contribution: 45 SCF conceived and designed the experiments. SCF, JCC, and MJW performed the 46 experiments and analyzed the data. JCC and MJW contributed equally to this work. 47 SCF wrote the paper. 48 49 50 51 Corresponding author: 52 Su-Chiung Fang 53 Biotechnology Center in Southern Taiwan, Academia Sinica, Tainan, 741, Taiwan 54 E-mail address: [email protected] 55 56 57 58 59 60



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ABSTRACT 61 62 The distinct reproductive program of orchids provides a unique evolutionary model 63 with pollination-triggered ovule development and megasporogenesis, a modified 64 embryogenesis program resulting in seeds with immature embryos, and mycorrhiza-65 induced seed germination. However, the molecular mechanisms that have evolved to 66 establish these unparalleled developmental programs are largely unclear. Here, we 67 conducted comparative studies of genome-wide gene expression of various 68 reproductive tissues and captured the molecular events associated with distinct 69 reproductive programs in Phalaenopsis aphrodite. Importantly, our data provide 70 evidence to demonstrate that protocorm-like-body (PLB) regeneration (the clonal 71 regeneration practice used in the orchid industry) does not follow the embryogenesis 72 program. Instead, we propose that SHOOT MERISTEMLESS (STM), a class I 73 KNOTTED-LIKE HOMEOBOX (KNOX) gene, is likely to play a role in PLB 74 regeneration. Our studies challenge the current understanding of the “embryonic” 75 identity of PLB. Taken together, the data obtained establish a fundamental framework 76 for orchid reproductive development and provide a valuable new resource to enable 77 prediction of gene regulatory networks that is required for specialized developmental 78 programs of orchid species. 79 80 81 82 83



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INTRODUCTION 84 Orchids have a very unique reproductive program. Unlike most flowering 85

plants, whose ovules and embryo sacs are fully developed and whose egg cells are 86 ready to be fertilized at anthesis, in some orchids, development of the ovule and 87 embryo sac is triggered by pollination (Withner, 1959; Arditti, 1992; Yeung and Law, 88 1997). Pollination and fertilization are separated by relatively long periods during 89 which the ovule and embryo sac develop. These periods vary among species and can 90 span from as little as 4 days in Gastrodia elata to 10 months in Vanda suavis (Arditti, 91 1992). After fertilization, embryogenesis of the vast majority of orchids lack 92 characteristic organogenesis and the embryos are arrested at the globular stage as 93 seeds continue to mature and desiccate (Raghavan and Goh, 1994; Yu and Goh, 2001; 94 Kull and Arditti, 2002). As a result, matured embryos of orchids do not have the 95 embryonic leaves (cotyledons) and embryonic roots commonly established in other 96 seed plants (Arditti, 1992; Dressler, 1993; Burger, 1998). Despite the incomplete 97 morphogenesis, orchid embryos possess axis polarity and complete maturation and 98 desiccation processes (Yeung et al., 1996; Lee et al., 2007; Lee et al., 2007; Lee et al., 99 2008). 100

The plant embryo is a miniature sporophyte developed from the zygote after 101 fertilization. Plant embryogenesis is a genetically defined program comprising 102 sequential developmental processes that result in a mature embryo in which the 103 structural and functional organization of the adult plant is established. Two distinct 104 but overlapping phases, morphogenesis and maturation take place during 105 embryogenesis (Bentsink and Koornneef, 2008; Braybrook and Harada, 2008). Basic 106 body-plan including organization of apical-basal polarity, formation of functionally 107 organized domains, and cell differentiation and tissue specification are established 108 during morphogenesis (Steeves and Sussx, 1989). Transcriptional regulators and 109 signaling components are important to control axis polarity and the cell division plane 110 (Jeong et al., 2012; Ueda and Laux, 2012). As morphogenesis approaches completion, 111 embryos cease to grow and macromolecules start to be synthesized and accumulated 112 as storage reserves. Abscisic acid (ABA) plays an important role and is coordinated 113 with a battery of transcriptional factors such as ABSCISIC ACID INSENSITIVE3 114 (ABI3), FUSCA3 (FUS3), LEAFY COTYLEDON 1 (LEC1), and LEC2 to regulate 115 accumulation of storage reserve and timely acquisition of the desiccation processes 116 (Suzuki et al., 2003; Gazzarrini et al., 2004; Finkelstein et al., 2005; Kagaya et al., 117



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2005; Kagaya et al., 2005). Failure to complete the maturation program in developing 118 seeds leads to ABA insensitivity, desiccation intolerance, reduced storage reserves, 119 and/or precocious germination (Koornneef et al., 1984; Finkelstein and Somerville, 120 1990; Nambara et al., 1992; Lotan et al., 1998; Luerssen et al., 1998). 121

Germination and early seedling development of orchid seeds is not a 122 spontaneous process and often requires species-specific mycorrhizal colonization 123 (Smith and Read, 2008; Waterman and Bidartondo, 2008). It has been proposed that 124 mycorrhizal colonization provides phosphate, nitrogen, or other mineral nutrients to 125 support seed germination (Leake, 1994; Rasmussen, 2002). Orchid seeds germinate 126 and form small spherical tuber-like bodies referred to as protocorms. Unlike the vast 127 majority of plants whose growth axes (shoot and root meristems) are established early 128 during embryo development, the protocorm has only one meristematic domain at the 129 anterior end where new leaves and roots are formed sequentially (Nishimura, 1981). 130 Because protocorm development initiates organogenesis that is absent during the 131 morphogenesis program of orchid embryogenesis, protocorm development is 132 sometimes considered to be a continuum of zygotic embryogenesis (Jones and 133 Tisserat, 1990; Ishii et al., 1998). However, the embryonic status of protocorms 134 remains to be determined. 135

Protocorm-like bodies (PLB) resemble protocorms structurally and are 136 triggered from explants and/or calluses (Jones and Tisserat, 1990; Chugh et al., 2009). 137 During the initiation of PLBs, callus cells from the explant form compact regions that 138 are composed of merstemoids (promeristems) (Lee et al., 2013). Polarized growth 139 starts from the surface cells of each compact pool of meristemoids. Continued cell 140 division produces anterior smaller cells that give rise to the shoot pole of a PLB and 141 posterior larger and vacuolated cells that form at the base of a PLB (Lee et al., 2013). 142 The first leaf is formed from the shoot pole of the PLB and the root is usually 143 produced at the base of the first leaf (Hong et al., 2008). Sometimes roots initiate 144 from the middle or bottom of the PLB body. As the clonal propagation of PLBs can 145 be multiplied by cutting, it has become a routine practice in the orchid floriculture 146 industry to generate clonal plantlets (Yam and Arditti, 2009). 147

Because the protocorm is considered to be an extended state of the zygotic 148 embryo, initiation and development of PLBs is referred to as somatic embryogenesis 149 (Begum et al., 1994; Chang and Chang, 1998; Ishii et al., 1998; Chen and Chang, 150 2006; Zhao et al., 2008; Lee et al., 2013). However, molecular evidence supporting 151



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such a hypothesis remains limited. Here we describe genome-wide gene activity in 152 ovary tissues containing developing ovules and embryos from fertilization to maturity 153 as well as in protocorm and PLB tissues of Phalaenopsis aphrodite. Our study reveals 154 that the molecular components required for plant ovule and embryo development are 155 evolutionarily conserved in P. aphriodite, and provides new insights into the 156 molecular dynamics that characterize the reproductive program of Phalaenopsis 157 orchids. Moreover, our data show that protocorms and PLBs share similar 158 transcriptomic signatures that are mostly different from those of zygotic embryos. 159 Furthermore, initiation and developmental processes of orchid PLBs do not follow the 160 somatic embryogenesis program but instead show a distinct regeneration program. 161 We report that SHOOT MERISTEMLESS, a class I KNOTTED-LIKE HOMEOBOX 162 gene, is likely to play an important role in PLB regeneration. Our studies challenge 163 the current understanding of the “embryonic” identity of PLB and suggest an 164 alternative pathway for PLB regeneration. 165 166 167



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RESULTS 168 De novo transcriptome assembly 169

To ensure full-spectrum coverage of transcripts whose expression is 170 important/required for general and tissue-specific proliferation and maintenance of 171 meristematic tissues, a reference transcriptome library was generated by paired-end 172 sequencing mRNA populations collected from different meristematic tissues 173 including developing ovaries containing developing ovules collected at 30, 40, 50, 60 174 days after pollination (DAP, Fig. 1A and Supplemental Fig. S1) and developing 175 embryos collected at 70, 80, 90, 100, 120, 140, 160, 180, and 200 DAP (Fig. 1A and 176 Supplemental Fig. S1), developing protocorms (Fig. 1B), developing PLBs (Fig. 1C), 177 newly emerging young leaves (< 2 cm), emerging stalk buds (< 2 cm), 5-10 cm floral 178 stalks, root tips (< 2 cm), and floral buds (<5 mm). The total size of the assembly was 179 ~117 Mb. A summary of assembly statistics is listed in Supplemental Table S1. This 180 assembly yielded 112,467 unigenes that are longer than 200 nt with a mean unigene 181 size of 1038 nt and a maximum unigene size of 15,584 nt. This transcriptome 182 provides the comprehensive transcript repertoire from various P. aprhodite meristems. 183 184 Different sets of co-expressed genes characterize reproductive development in P. 185 aphrodite 186

To compare the transcriptome dynamics of protocorms, PLBs, ovary tissues 187 spanning from ovule development to embryogenesis, young leaves, stalk buds, and 188 floral stalks, 10 Mb single end mRNA reads from each group of tissues (see Materials 189 and Methods) were mapped to the assembled reference transcriptome and analyzed by 190 principal component analysis (PCA). The mapping read analyses are summarized in 191 Supplemental Table S2. Four distinct groups were identified by the analysis (Fig. 192 2A): (I) Ovaries containing developing ovules (30-40 and 50-60 DAP) and 193 developing embryos (70-80 and 90-100-120 DAP); (II) Ovaries containing maturating 194 embryos (140-160 DAP and 180-200 DAP); (III) protocorms and PLBS; and (IV) 195 young leaves, emerging stalk buds, and floral stalks. Developmental time frames 196 identified as being closely associated are likely to share the greatest similarity in 197 overall gene expression and are therefore likely to share cellular functions. 198

We were interested in understanding the extent to which gene expression was 199 coordinated during developmental periods such as fertilization, embryo development, 200 seed maturation, and protocorm and PLB development. K-mean analysis was applied 201



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to the RNA-seq dataset to identify genes whose expression was preferentially 202 enriched in specific tissues. To reduce false-positive results, only transcripts 203 expressed (FPKM ≥ 5) in at least one tissue were selected. To increase the stringency, 204 an equal to or greater than tenfold change in at least two tissues was chosen as a 205



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cutoff. Twelve clusters representing stage-specific or tissue-specific enriched 206 transcripts were identified (Supplemental Fig. S1B) and listed in Supplemental Table 207 S3. These transcripts encode a range of functional categories, although some of the 208 encoded proteins had no known functions (Supplemental Data Set 1). Gene ontology 209 (GO) category enrichment analysis was applied to these clusters to identify 210 predominant cellular processes associated with developing ovaries, protocorms, and 211 PLBs (Fig. 2B and Supplemental Data Set 2). The detailed list of clustered transcripts 212 and their GO terms are given in Supplemental Data Set 1. 213

After pollination as the ovary started to develop at 30-40 DAP (Supplemental 214 Fig. S1B, I), transcripts associated with cell-cycle-associated biological processes 215 such as the cell cycle, cytokinesis by cell plate formation, DNA replication initiation, 216 microtubule cytoskeleton organization, cell division, and regulation of cell cycle are 217 strongly enriched (Fig. 2B). As development proceeded to 50-60 DAP (Supplemental 218 Fig. S1B, II), genes involved in metal ion transport, phosphoenolpyruvate 219 carboxykinase activity, and serine-type peptidase activity were represented (Fig. 2B). 220 At around 70-80 DAP (Supplemental Fig. S1B, III), when fertilization had occurred 221 and embryos started to develop in ovary tissues (Nadeau et al., 1996; Lee et al., 2008), 222 production of siRNA involved in RNA interference, DNA methylation, and 223 methyltransferase activity were overrepresented (Fig. 2B). As embryos continued to 224 develop in ovaries at 90-100-120 DAP and 140-160 DAP (Supplemental Fig. S1B, IV 225 and V), transcripts encoded by genes associated with catabolism and macromolecular 226



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transport and storage such as lipid transport, carbohydrate transport, DNA catabolic 227 processes, and sugar transmembrane transporter activity were significantly enriched 228 (Fig. 2B). As the ovary reached maturity (Supplemental Fig. S1B, VI and Fig. 3B), 229 transcripts of genes involved in antiporter activity, the ubiquitin ligase complex, and 230 the oxidation-reduction process were enriched (Fig. 2B). 231

GO analysis of the K-mean cluster VII, VIII, and IX revealed that cellular 232 processes involved in oxidation-reduction processes, heme binding, peroxidase 233 activity, and copper ion binding were strongly enriched in both protocorms and PLBs 234 (Supplemental Fig. S1B and Fig. 2B). Transcripts encoded by genes associated with 235 terpene synthase activity, lyase activity, nucleoside-triphosphatase activity, lipid 236



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metabolic processes, and the abscisic acid-activated signaling pathway were 237 significantly enriched only in PLB tissues. 238 239 Transcription factors enriched before, during, and after fertilization in ovary 240 tissues 241

To survey the regulatory network controlling developmental transitions during 242 orchid reproductive development, we used the GO category of “regulation of 243 transcription, DNA-templated” to identify tissue- or stage-specific transcription 244 factors (TFs) enriched in each cluster (Supplemental Data Set 3 and Table 1). 245 Transcripts of Arabidopsis orthologs previously shown to regulate carpel and ovule 246 development such as AGAMOUS (PaMADS1 and PaMADS61), SEPALLATA 247 (PaMADS13), AINTEGUMENTA (PaANT), CUP SHAPE COTYLEDON (PaCUC), 248 and SPATULA (PaSPT) (Elliott et al., 1996; Favaro et al., 2003; Pinyopich et al., 249 2003; Brambilla et al., 2007; Nahar et al., 2012; Galbiati et al., 2013) were 250 overrepresented in ovary tissues collected from 30 to 60 DAP during which ovules 251 were developing. A homeobox TF O39, previously isolated as an ovule specific 252 cDNA of Phalaenopsis orchid (Nadeau et al., 1996), was also identified in our dataset 253 (PaHD-Zip4, Table 1). The nomenclature of MADS domain transcription factors of P. 254 aphrodite follows that of Phalaenopsis equestris (Cai et al., 2015). Three additional 255 MADS domain factors, PaMADS61, PaMADS62, and PaMADS63 were identified in 256 this study (Supplemental Fig. S2A). 257

As ovary development proceeded to 70-80 DAP, when fertilization occurred, 258 mRNAs of four MADS domain (PaMADS7-SHATTERPROOF/SEEDSTICK-like, 259 PaMADS39, PaMADS51, and PaMADS63) and three homeodomain-leucine zipper 260 (HD-Zip) family TFs were found to be enriched (Table 1). The expression patterns of 261 selected transcripts listed in Table 1 were confirmed independently by quantitative 262 reverse transcription polymerase chain reaction (qRT-PCR, Fig. 3A). The 263 phylogenetic relationship of the identified orchid proteins and their Arabidopsis 264 counterparts is shown in Supplemental Fig. S2A, S2B and S2C. 265

As ovary development proceeded from 90 to 200 DAP, many seed specific 266 TFs such as BABY BOOM (PaBBM), LEAFY COTYLEDON 1 (PaLEC1), FUSCA3 267 (PaFUS3), ABSISIC ACID INSENSITIVE3 (PaABI3L1 and PaABI3L2), and 268 WRINKLED1 (PaWRI1) were preferentially expressed (Table 1). The identities of 269 these embryonic marker genes were supported by phylogenetic analysis 270



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(Supplemental Fig. S2B and S2D) and sequence alignment (Supplemental Fig. S3). 271 Quantitative RT-PCR confirmed that mRNAs of PaBBM, PaLEC1, PaABI3L1, 272 PaABI3L2, and PaFUS3, started to accumulate in ovary tissues at 100 DAP and 273 reached a peak at 180 DAP (Fig. 3B). The expression pattern of PaWRI1 mRNA 274



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followed a similar pattern except its accumulation peaked at 160 DAP. The 275 maturation status of the developing seeds was marked by expression of two seed 276 maturation markers, OLEOSIN1 (PaOLE1) and PaOLE2 (Table 1 and Fig. 3B). 277 Preferential accumulation of PaBBM and PaLEC1 mRNAs in developing embryos 278



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were further confirmed by in situ hybridization, with both mRNAs starting to 279 accumulate in developing embryos eighty days after pollination (early stage of seed 280 development, Fig. 4A). PaBBM mRNA level continued to increase from 110 to 180 281 DAP and reached a peak when embryos approached the end of maturation. PaLEC1 282 mRNA on the other hand reached a peak in embryos at 140 DAP and was maintained 283 at relatively high level from 160 to 180 DAP. 284 285 Two 7S globulins are preferentially accumulated in developing seeds. 286

During orchid seed development, storage proteins are synthesized and form 287 protein bodies in developing embryos (Lee et al., 2006; Yang and Lee, 2014). We 288 were interested to learn the compositions of the protein reserve and surveyed the 289 expression patterns of the major seed storage protein, albumins, globulins, and 290 prolamins (Shewry et al., 1995). At least one 11S globulin and four 7S globulins were 291 identified from our transcriptome database and their transcript abundance is shown in 292 Table I. The phylogenetic relationship of the full-length proteins encoded by the 11S 293 globulin and two 7S globulins is shown in Supplemental Fig. S4. Notably, transcripts 294 of two 7S globulin genes, Pa7S-1 and Pa7S-2, steadily accumulated during the seed 295 maturation process with a peak at 180 DAP (Fig. 3B), suggesting they are the major 296 storage proteins in orchid seeds. In addition to developing seeds, Pa7S-1 mRNA was 297 extremely abundant in protocorms. Intriguingly, prolamin and 2S albumin, the storage 298 proteins commonly found in endosperms, were not identified in our transcriptome 299 database and two publicly available orchid transcriptome databases (Su et al., 2013; 300 Cai et al., 2015). 301

302 Embryonic specific markers are not enriched in protocorm and PLB tissues 303

Expression of embryonic markers such as BBM, LEC1, FUS3, and ABI3s are 304 not only enriched in zygotic and somatic embryos, some of their functions have also 305 been demonstrated to be sufficient to establish embryonic fate during somatic 306 embryogenesis (Braybrook and Harada, 2008; Smertenko and Bozhkov, 2014). 307 Unlike somatic embryonic tissues observed in other plant species, PaLEC1 and 308 PaFUS3 mRNAs were hardly detectable in protocorms and PLBs. The mRNAs of 309 PaBBM and PaABI3L2 accumulated to low levels in 10-day-old protocorms and were 310 hardly detectable in developing PLBs (Table 1 and Fig. 3B). The level of PaABIL1 311 mRNA was relatively high in abundance in developing protocorms and low in 312



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abundance in developing PLBs (Table 1 and Fig. 3B). In addition, mRNAs of the two 313 embryonic marker genes, PaWRI1 and PaOLE1 whose functions are important for 314 accumulation of storage reserves during the maturation phase of embryogenesis 315 (Cernac and Benning, 2004; Hsieh and Huang, 2004) were expressed in very low 316 abudance or undetectable in developing protocorms and PLBs. In situ hybridization 317 also confirmed the lack of detectable PaLEC1 and PaBBM mRNA in developing 318 PLBs (Fig. 4B and 4C). Therefore, expression of the embryonic marker genes was not 319 correlated with initiation and development of PLBs. 320

The ability of PaLEC1 and PaBBM to induce somatic embryogenesis was 321 verified in Arabidopsis. Expression of the PaBBM and PaLEC1 proteins was verified 322 by western blot analysis (Supplemental Fig. S5A). Overexpression of 35S:PaBBM-323 eGFP or 35S:eGFP- PaLEC1/35S:PaLEC1-eGFP (Fig. 5A and 5B) but not the 324 empty vector (Supplemental Fig. S5B and S5C) caused ectopic production of 325 cotyledons from somatic tissues. The embryonic specific genes such as Ole, Coleosin, 326 Cruciferin 3 (CRU3), ABI3, and FUS3 were upregulated in somatic embryonic culture 327 tissues of the transgenic plants (Fig. 5C and 5D). In addition, triacylglycerols that 328 accumulate in embryonic tissues and stained intensely with the Sudan Red 7B, were 329 also accumulated in embryonic-like tissues of 35S:PaLEC-eGFP and 35S:eGFP-330 PaBBM transgenic lines (Fig. 5E). Moreover, overexpression of eGFP-PaLEC1 331 rescued lec1-1 desiccation tolerant phenotype (Fig. 5E), supporting that PaLEC1 is 332 the functional ortholog of Arabidopsis LEC1. The 35S:eGFP-PaBBM construct failed 333 to be generated and was therefore omitted from this study. In short, PaLEC1 and 334 PaBBM genes are evolutionarily conserved and capable of inducing the somatic 335 embryonic program. 336



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In addition to surveying transcriptional factors that displayed enriched 337 expression pattern during seed development, we also examined SOMATIC 338 EMBRYOGENESIS RECEPTOR KINASE (SERK) whose expression has been shown 339 to be associated with somatic embryogenesis (Schmidt et al., 1997; Hecht et al., 2001; 340



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Santos et al., 2005; Steiner et al., 2012). Three previously reported SERK-like genes, 341 PaSERK1, PaSERK2, and PaSERK5 (Huang et al., 2014), were also present in our 342 transcriptome database. However, expression of PaSERK1, PaSERK2, and PaSERK5 343 was ubiquitous across the tissues we analyzed and did not display embryonic-specific 344



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patterns (Table 1). The lack of correlation between embryonic/somatic embryonic 345 tissues and expression of SERK genes has been reported in rice and maize (Baudino et 346 al., 2001; Ito et al., 2005). 347 348



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Expression of PaSTM is associated with PLB development 349 Knowing PLB development does not follow the embryogenesis program, we 350

were interested in genes whose functions may potentially contribute to PLB initiation 351 and development and provide hints about pathway(s) from which the PLB is derived. 352 To do that, TF genes under the GO category “regulation of transcription, DNA-353 templated” in PLB clusters (Supplemental Fig. S1B) were identified (Supplemental 354 Data Set 3). 355 Among the PLB-enriched TFs, we were particularly interested in class-1 356 KNOX TF PaSTM because ectopic expression of class-1 KNOX TFs has been reported 357 to cause formation of new tissue-organization centers that are sufficient to induce 358 shoots or organ-related structures (Sinha et al., 1993; Chuck et al., 1996; Williams-359 Carrier et al., 1997; Golz et al., 2002). PaSTM encodes a protein that shares 63% 360 identity and 73% similarity to Arabidopsis STM. Phylogenetic analysis of class-1 361 KNOX TFs shows that PaSTM and Arabidopsis STM comprise a paired clade 362 (Supplemental Fig. S6A). The expression level of PaSTM mRNA was correlated with 363 initiation of PLB being significantly elevated at the early stage of PLBs (small), and 364 declining but being maintained at moderate levels as development proceeded (30 days 365 after germination, Fig. 6A). The level of PaSTM mRNA, on the other hand, was 366 relatively low in 10- and 20-day-old protocorms and increased to a moderate level in 367 30-day-old protocorms. Coincidently, the expression pattern of PaSTM was positively 368 correlated with its potential target, the Gibberellin 2-oxidase1 (PaGA2OX1, Fig. 6A). 369 Maize STM homolog, KNOTTED1, has been shown to directly regulate GA2 oxidase 370 to maintain a low level of GA in shoot apical meristems (Bolduc and Hake, 2009). In 371 addition, accumulation of PaSTM in PLBs was positively correlated with a shoot 372 generation marker (Che et al., 2006), PaERF1 (homologous to Arabidopsis RAP2.6L 373 ERF/AP2 transcription factor, Fig. 6A and Supplemental Fig. S6B), suggesting that 374 PLBs have a shoot generation capacity. The expression of PaERF1 did not seem to be 375 a general stress-related response because the mRNA of the PaERF2, a stress-related 376 gene (Supplemental Fig. S6B), showed a different expression pattern. In situ 377 hybridization further confirmed that PaSTM mRNA was evenly distributed in newly 378 emerging and small-size PLBs but was undetectable in highly vacuolated callus cells 379 (Fig. 6B). In developing protocorms, on the other hand, PaSTM mRNA was restricted 380 to the anterior end where shoots initiate (Fig. 6C). Taken together, the results showed 381 that expression of PaSTM mRNA is tightly associated with initiation of PLBs. 382



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To exclude the possibility of involvement of PaLEC1 and PaFUS3 during 383 PLB initiation, expression of PaLEC1 and PaFUS3 was also examined in newly 384 emerging PLBs (PLBN). Unlike high levels of PaLEC1 and PaFUS3 mRNAs 385 detected in embryonic tissues at 160 DAP, PaLEC1 and PaFUS3 mRNAs were 386 almost undetectable in developing PLBs including PLBN (Fig. 6D). This result 387 confirms that expression of PaLEC1 and PaFUS3 is not associated with PLB 388 initiation. The preferential expression of PaSTM in PLBN was validated by qRT-PCR 389 analysis (Fig. 6D). WUSCHEL (WUS) is reported to act as a positive regulator of 390 shoot stem cell fate (Gordon et al., 2007; Duclercq et al., 2011). Phalaenopsis 391 WUSCHEL (PaWUS) and WUS-related Homeobox (PaWOX) gene were identified 392 from our transcriptome database (Supplemental Fig. S6C). However, PaWUS and 393 PaWOX mRNAs were not upregulated in PLBs (Table 1). It is possible that 394 expression of PaWUS is restricted to a defined area of PLB meristem and its potential 395 role to PLB development remains to be determined. 396

To test the ability of PaSTM to induce PLB-like organogenesis, we generated 397 transgenic Arabidopsis plants overexpressing PaSTM or its fusion to a GFP protein 398 (GFP-PaSTM or PaSTM-GFP). Expression of the PaSTM proteins was confirmed by 399



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immunoblot (Fig. 7A). Compared to the transgenic plant carrying the empty vector 400 (Fig. 7B), most of the T1 transgenic plants overexpressing PaSTM grew very slowly 401 and had severe developmental defects. Among the 237 T1 transformants we 402 recovered, most displayed aborted normal postembryogenic development and initiated 403



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unorganized cell proliferation with 116 plants (49.4%) forming a markedly large 404 dome-shaped structure (Fig. 7C) and 101 plants (43.0%) forming a brush-like 405 disorganized structure (Fig. 7D) at the position where shoot meristems resided. The 406 first two rosette leaves of overexpressors were severely deformed and displayed either 407 a slender or lobed structure (Fig. 7E). Most of these plants arrested at the seedling 408 stage. Very few transgenic plants managed to make a few more leaves and bolted 409 approximately 35 to 37 days after germination (Fig. 7F). The rest of the other 410 transgenic lines (7.6%) grew like wild-type (wt). To exclude the potential influence of 411 antibiotic on transgenic plant overexpressing PaSTM, T1 transgenic plants that were 412 kept off antibiotics 10 days after germination were examined. Phenotypes similar to 413 transgenic plants kept on the antibiotics were observed (Supplemental Fig. S7A). 414 Homozygous T2 lines from wt-looking 35:GFP-PaSTM overexpressors were 415 recovered for further analysis. Unlike their heterozygous counterparts, leaf blades of 416 cauline and rosette leaves of homozygous lines appeared to be curved and lobed and 417 petioles were shorten (Fig. 7G), which are similar to previous reports on transgenic 418 plants overexpressing class-1 KNOX TFs (Chuck et al., 1996; Sakamoto et al., 1999; 419 Ori et al., 2000). However, we did not observe ectopic meristems from PaSTM 420 overexpressors probably because of structural divergence of STM between 421 Phalaenopsis orchids and Arabidopsis. Similar to 35S:PaSTM transgenic lines, 422 35:GFP-PaSTM overexpressors displayed large dome-shaped or brush-like shoot 423 apical meristems (Supplemental Fig. S7B). A less severe phenotype was observed in 424 35S:PaSTM-GFP overexpressors (Supplemental Fig. S7C). None of the described 425 phenotypes was observed in vector-only control plants (Supplemental Fig. S7D). 426

The shoot regeneration capacity of the unorganized structures of PaSTM 427 overexpressors was monitored by the expression of the shoot regeneration markers 428 RAP2.6L and GA2 oxidase2 (GA2OX2) (Che et al., 2006). As shown in Fig. 7H, 429 mRNAs of these markers were increased in abundance in PaSTM overexpressors but 430 not in the wt or transgenic plants carrying the empty vector. Additionally, the 431 RAP2.6L mRNA level was positively correlated with severity of abnormality of 432 PaSTM overexpressors. Taken together, we propose that PaSTM may be an important 433 factor for PLB generation. 434 435 436



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DISCUSSION 437 Transcriptome dynamics of pollination-triggered reproductive development 438 Here, we profiled temporal transcriptome dynamics in developing ovaries as 439 development progressed from ovule to embryo development. The data revealed that 440 distinct cellular functions were associated with different stages of the Phalaenopsis 441 reproductive program. Cell division-related gene activities were overrepresented at 442 the early stage of ovary development during which ovules and pollen tubes were 443 developing. This is consistent with our previous finding that the selected core cell-444 cycle genes are preferentially expressed in ovaries transitioned from gametophyte 445 development to embryogenesis (Lin et al., 2014). In addition, TFs such as AGAMOUS 446 (AG)-, AINTEGUMENTA (ANT)-, BELL1 (BEL1)-, CUP SHAPE COTYLEDON 447 (CUC)-, SEPALLATA (SEP)-, and SPATULA (SPT)-like genes previously shown to 448 regulate carpel and ovule development in Arabidopsis were enriched in ovary tissues 449 before transition. It has been shown that CUCs work together with SPT to control 450 formation of carpel marginal structures and development of septa and ovules (Nahar 451 et al., 2012; Galbiati et al., 2013). ANT and CUCs are important for initiation of the 452 ovule primodium (Ishida et al., 2000; Galbiati et al., 2013). BEL1 is important to 453 control integument identity and works together with AG and SEP to regulate ovule 454 development (Modrusan et al., 1994; Ray et al., 1994; Reiser et al., 1995; Brambilla 455 et al., 2007). Ovule fate is further maintained by members of the MDAS-box family 456 of TFs, SHP1, SHP2, STK, and AG (Favaro et al., 2003; Pinyopich et al., 2003). 457 Taken together, our results indicate that ovule development of Phalaenopsis orchids 458 requires similar sets of regulatory factors and is likely to be evolutionarily conserved. 459

The RNA-seq analysis revealed that DNA methylation, RNAi interference, 460 and methione biosynthetic processes marked the stage when fertilization occurred and 461 embryos began to develop. Epigenetic reprogramming involved in small RNA-guided 462 methylation and DNA methylation has been reported to maintain genome integrity 463 and epigenetic inheritance in reproductive tissues (Calarco et al., 2012; Jullien et al., 464 2012) and is likely to play a role during the reproductive development of 465 Phalaenopsis orchids. 466

As embryos started to develop and seeds began to form (90 to 200 DAP), seed 467 specific TFs including PaLEC1, PaFUSCA3, PaABI3L1, PaABI3L2, PaBBM and 468 PaWRI1 were identified as overrepresented transcripts. In addition, enrichment of GO 469 terms associated with lipid and carbohydrate mobilization and storage at the late stage 470



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of developing ovary tissues (140-160 DAP and 180-200 DAP) confirms the 471 concurrent seed maturation processes (Fig. 2B and supplemental Data Set 2). The 472 tissue-specific localization and functional studies of PaLEC1 and PaBBM validates 473 their roles in activating and maintaining the embryonic program. Interestingly, the 474 major shift in gene expression between early and late seed development (Fig. 2A) 475 indicates maturation-specific transcriptome reprogramming, which has been also 476 reported in Arabidopsis (Belmonte et al., 2013). Interestingly, a substantial overlap in 477 RNA populations of ovary tissues progressing from ovule development to early 478 embryo establishment (Fig. 2A and Fig. 3A, cluster X) suggests that similar cellular 479 processes are likely to be shared as tissues transitioned from gametophytic to 480 embryonic development in Phalaenopsis orchids. Taken together, global comparisons 481 of mRNA populations suggested a coordinated temporal shift in gene expression 482 during reproductive development in ovary tissues. Although lacking the complete 483 organogenesis and histodifferentiaion, the maturation process of Phalaenopsis orchid 484 embryos characterized by seed specific TFs is evolutionarily conserved. 485

One of the distinct features of orchid seeds is their lack of endosperms. It has 486 been documented that triple fusion between polar nuclei and sperm nucleus rarely 487 occurs and endosperm development is either aborted at very early stage or cannot be 488 initiated (Kull and Arditti, 2002; Batygina et al., 2003). Coincidently, transcripts of 489 the storage proteins 2S albumin and prolamins commonly found in endosperms of the 490 monocotyledon plants (Shewry and Halford, 2002) could not be identified from our 491 and publicly available transcriptome databases. Intriguingly, members of type I 492 MADS box transcription factors, whose functions are found to be associated with 493 endosperm development (Masiero et al., 2011), are greatly reduced in orchid genomes 494 (Cai et al., 2015; Lin et al., 2016; Zhang et al., 2016). The concurrent loss of the 495 molecular repertoire normally associated with endosperm development may 496 contribute to the lack of endosperm in orchid seeds. 497 498 Regulatory network controlling genes expressed during embryo development are 499 different from those of the PLB and protocorm 500

Our studies provide evidence to support that protocorms and PLBs shared 501 similar transcriptome dynamics. Particularly, chloroplast development and functions 502 involved in heme binding, copper binding, and the oxidation-reduction process were 503 overly active. In addition, stress-related cellular processes including the abscisic acid-504



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activated signaling pathway and wounding response were overrepresented. It is likely 505 that cutting and the culture conditions activate stress responses during tissue culture 506 practice, as suggested previously (Fehér et al., 2003; Bai et al., 2013; Gliwicka et al., 507 2013; Maximova et al., 2014). 508

Surprisingly, protocorms and PLBs (often described as somatic embryos in 509 literatures) shared little similarity to zygotic embryonic tissues or other meristematic 510 tissues like emerging young leaves, emerging stalk buds, and floral stalks (Fig. 2A). 511 The lack of embryonic identity in PLB was further supported by lack of RNA 512 accumulation of two embryonic specific marker genes, PaLEC1 and PaBBM. 513 Therefore, protocorm and PLB seem to possess a unique molecular program that is 514 different from embryonic and other meristematic tissues. 515

Our data show that PLB and protocorm development seems to be regulated 516 similarly but not identically. For example, PaABI3L1 mRNA was relatively abundant 517 in protocorms but its level was low in PLBs (Fig. 3B). PaSTM, PaGA2OX1, and 518 PaERF1 mRNAs, on the other hand, were relatively abundant in PLB but less 519 abundant in protocorms (Fig. 6A). Functional characterization of these genes may 520 help identifying gene regulatory networks unique to protocorms or PLBs. 521 522 Protocorm-like bodies: organogenesis vs. somatic embryogenesis 523

Somatic embryogenesis is a defined developmental process that leads to 524 establishment of embryos independent of fertilization event (von Arnold et al., 2002; 525 Braybrook and Harada, 2008; Yang and Zhang, 2010). Similar to zygotic 526 embryogenesis, specific molecular markers contributing to formation of basic body 527 plan (morphogenesis) and accumulation of seed storage macromolecules (maturation) 528 are commonly used to define somatic embryogenesis process. Despite the commonly 529 accepted view in the orchid community that PLBs are of somatic embryonic nature, 530 the comparative transcriptome and marker gene analyses presented here argue that 531 regeneration of PLBs does not follow the embryogenesis program. Instead, the tight 532 correlation between PLB development and PaSTM expression suggests that the 533 PaSTM-mediated shoot organogenesis pathway may be important for PLB initiation. 534

Expression of STM has been reported to be associated with organogenic shoot 535 formation of Kalanchoe, Agave, and dodder (Garcês et al., 2007; Abraham-Juárez et 536 al., 2010; Alakonya et al., 2012). Upregulation of STM gene is also associated with de 537



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novo assembly of shoot apical meristems from cultured explants (Gordon et al., 2007; 538 Atta et al., 2009). Similarly, de novo leaf initiation of river weeds that lack typical 539 shoot apical meristems is tightly linked to the expression of the STM gene (Katayama 540 et al., 2010). The positive role of class-1 KNOX genes on meristem cell fate is further 541 supported by the gain-of-function approach. In these cases, ectopic expression of the 542 class-1 KNOX genes has been found to cause formation of new tissue-organization 543 centers that are sufficient to induce ectopic shoots or organ-related structures (Sinha 544 et al., 1993; Müller et al., 1995; Chuck et al., 1996; Williams-Carrier et al., 1997; 545 Brand et al., 2002; Golz et al., 2002; Lenhard et al., 2002). Consistently, PaSTM is 546 able to increase shoot generation ability by promoting expansion of shoot apical 547 meristems and/or inducing organ-related structures with concurrent upregulation of 548 shoot regeneration makers, RAP2.6L and GA2 oxidase2, when overexpressed in 549 Arabidopsis. Based on these findings, we propose that PaSTM may be an important 550 factor for PLB regeneration. 551

During de novo organogenesis, initiation of cell division, establishment of 552 auxin maxima, and specification of founder cells are commonly observed before 553 organ development (Pernisova et al., 2009; Perianez-Rodriguez et al., 2014). In 554 addition, coordinated interaction of phytohormones such as auxin, cytokinin, and 555 gibberellins are known to regulate battery of genes required for the acquisition of 556 competence and/or for organization of shoot apical meristem (Benková et al., 2003; 557 Gordon et al., 2009; Pernisova et al., 2009; De Smet et al., 2010; Marhavy et al., 558 2011; Marhavy et al., 2014; Schuster et al., 2014). It is likely that similar signaling 559 and gene regulatory activities are important in setting up PLB regeneration. In fact, 560 expression of PaGA2OX1, a GA-catabolizing enzyme, was associated with PLB 561 development. This is consistent with previous reports that GA inactivation is required 562 for activity of the shoot apical meristem (Sakamoto et al., 2001; Jasinski et al., 2005; 563 Bolduc and Hake, 2009). Additionally, several auxin-responsive genes were found to 564 be upregulated in PLB tissues (Supplemental Dataset 1). It will be of future interest to 565 understand how phytohormone signaling is integrated with the transcription network 566 to coordinate the initiation and development of PLBs. 567

Unlike the de novo organogenesis commonly observed in other plant species 568 where organs such as shoots or roots are directly generated from callus-derived 569 meristematic tissues (Duclercq et al., 2011), wound-induced callus tissues of 570 Phalaenopsis orchids often if not entirely take the PLB route before subsequent shoot 571



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regeneration (Ernst, 1994). This raises the question of whether PLB is a specialized 572 form of organ with shoot meristem development. If this is the case, what are the 573 unique factors that contribute to PLB regeneration and how are they different from 574 those for direct shoot regeneration? The comprehensive transcriptome catalog of 575 developing PLBs presented here provides valuable resource and may help identifying 576 key genes to address theses questions. 577

In summary, in this study, we profiled the genome-wide transcriptome of 578 reproductive development in P. aphrodite. The temporal and spatial integration of 579 transcriptomic dynamics in reproductive tissues at different developmental stages 580 provide valuable insights into the gene regulatory programs that characterize the 581 reproductive processes of Phalaenopsis orchids. In addition, our findings uncover 582 previously unrecognized tissue identity of PLB. Furthermore, we propose that the 583 regeneration program of PLB is likely derived from a PaSTM-dependent regeneration 584 process. 585 586 Materials and Methods 587 Plant Materials and Growth Conditions 588 Phalaenopsis aphrodite Subsp. formosana (m1663) seedlings in 2.5- or 3-inch pots 589 were purchased from Chain Port Orchid Nursery (Ping Tung, Taiwan). Plants were 590 grown in a growth chamber with alternating 12 h light (23°C)/12 h dark (18°C) 591 cycles. Arabidopsis Columbia ecotype was grown at 22°C under 16 h light/8 h dark 592 cycles in a growth chamber. lec1-1 mutant (Lotan et al., 1998) was purchased from 593 the Arabidopsis Biological Resource Center (http://www.arabidopsis.org). 594 595 Induction of PLBs 596 The mature seeds were allowed to germinate on ¼ strength MS basal medium 597 supplemented with 0.1% (w/v) tryptone, 1.8% (w/v) sucrose, 2% (w/v) potato 598 homogenate, 0.00001% (w/v) thiamine-HCl, 0.00001% (w/v) pyridoxine-HCl, 599 0.0001% (w/v) nicotinic acid, 0.01% (w/v) myo-inositol, 1% (w/v) agar, and adjusted 600 to pH 5.7. Fifty-five to eighty days after germination, protocorms grown to 601 approximately 3 mm in diameter were excised to remove the tip and bottom portions. 602 The protocorm segments were transferred to PLB-inducing medium containing 0.1% 603 (w/v) tryptone, 2% (w/v) sucrose, 2% (w/v) potato homogenate, 2.5% (w/v) banana 604



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homogenate, 0.01% (v/v) citric acid, 0.1% (w/v) charcoal, 1% (w/v) agar, and 605 adjusted to pH 5.5 to induce primary PLBs. Primary PLBs were then used to induce 606 secondary PLBs by cutting to remove the tip and bottom portions. The PLB segments 607 were then moved to PLB-inducing medium as described above. Secondary PLBs were 608 used for the experiments described below. Cultures were maintained at 25°C under 16 609 h light/8 h dark cycles under illumination at 45 to 55 μmol photons m-2 s-1 in a growth 610 chamber. A thin layer of callus tissue formed on the cutting surface of explants before 611 appearance of emerging PLBs (Fig. 5B). 612 613 Sample collection and RNA extraction 614 Orchid flowers were hand pollinated and developing ovaries were harvested at the 615 specified day. For reproductive tissues, only the interior tissues of developing 616 capsules were scooped and pooled for RNA extraction (Fig. 1A and Supplemental 617 Fig. S1). Because PLBs did not grow at a synchronized rate, the size and 618 developmental stage of PLB samples were categorized and collected separately (Fig. 619 1B). Protocorms that germinated after 10-, 20- and 30-days were collected and 620 categorized (Fig. 1C). Because germination rate varied in different batches of 621 capsules, only healthy-looking protocorms (light-green in color and larger than the 622 ones that failed to develop) were individually collected for the experiments. Young 623 leaves, emerging stalk buds, or root tips with sizes smaller than 2 cm in length, 5-10 624 cm long floral stalks, and < 5 mm floral buds were collected for RNA extraction. 625 The tissues samples were flash frozen in liquid nitrogen and stored in a freezer at -626 80°C. RNA was isolated using OmicZol RNA Plus extraction reagent (Omics Bio) 627 according to the manufacturer’s instructions. The isolated total RNA was treated 628 with RNase-free DNase (Qiagen) followed by RNeasy mini-column purification 629 according to the manufacturer’s instructions (Qiagen). 630 631 Transcriptome assembly and RNA seq 632 RNA samples extracted from different tissues including interior tissues of 633 developing capsules (30, 40, 50, 60, 70, 80, 90, 100, 120, 140, 140, 160, 180, and 634 200 DAP), protocorms, PLBs, young leaves, emerging stalk buds, floral stalks, 635 floral buds, and root tips were pooled together for transcriptome sequencing. The 636 paired-end cDNA library was synthesized and amplified using the TruSeq RNA 637



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Sample Prep Kit (v2) following the manufacturer’s instructions (Illumina, USA). 638 The cDNA library was sequenced by Genome Hiseq2000 (Illumina, USA) 639 according to the supplier’s protocols (Welgene, Taiwan). The raw sequencing data 640 were filtered to remove low-quality (Quality Value ≥20), adaptor, and repeat 641 sequences (Smeds and Kunstner, 2011). Qualified reads were de novo assembled by 642 the Trinity program (Grabherr et al., 2011). The resulting sequences and paired end 643 information were connected and incorporated by SSPACE Basic v.2 (Boetzer et al., 644 2011) and extended by TGICL (Pertea et al., 2003) to generate unigenes. The 645 estimation of unigene abundance was calculated by RSEM (Li and Dewey, 2011). 646 RSEM computes maximum likelihood abundance estimates and posterior mean 647 estimates and calculates 95% credibility intervals for each gene and isoform. 648 Unigenes which have at least one expected count and effective length ≥ 200 nt were 649 included in the transcriptome assembly. The assembled 12GB sequence reads 650 yielded 112,467 unigenes. Raw sequenced reads and nucleotide assembled unigenes 651 were deposited in the GenBank database (SRA261547, and SUB930352). 652

Additional ~10 Mb 50 bp single end reads from interior tissues of developing 653 capsules (30-40 DAP, 50-60 DAP, 70-80 DAP, 90-100-120 DAP, 140-160 DAP, 180-654 200 DAP), protocorms, PLBs, young leaves, emerging stalk buds, and floral stalks 655 were sequenced separately by Genome Analyzer IIx (Illumina, USA). The RNA reads 656 were mapped to the assembled transcriptome using the short read alignment software 657 Bowtie 2 (Langmead and Salzberg, 2012). The relative abundances of the transcripts 658 were quantified by Cufflinks2 (Trapnell et al., 2012). Between 84 and 90% of RNA 659 reads derived from sampled tissues were able to be mapped back to the assembled 660 transcriptome (Supplemental Table S2). The gene expression levels were calculated 661 as fragments per kilobase of transcript per million mapped reads (FPKM). 662 663 Functional annotation of the assembled unigenes 664 The assembled unigenes were searched against the NCBI non-redundant protein (Nr) 665 database using the alignment algorithm RAPSearch2 (Zhao et al., 2012) with a cut-off 666 E-value ≤ -3. The top alignment hits were used to predict the sequence orientation and 667 Gene Ontology (GO) accessions of the unigenes. 668 669 Data analyses and co-expression clustering 670



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PCA analyses were performed using GeneSpring12.6.1 software. To reduce the false-671 positive result caused by low abundance transcripts and generate robust groups of 672 coregulated genes, transcripts with a FPKM value larger or equal than 5 in at least one 673 tissue and showed 10 fold difference in at least two different tissues were selected for 674 clustering. Identification of co-regulated mRNAs was performed using 675 MultiExperiment Viewer (MeV) software (Howe et al., 2011). K-mean support using 676 Pearson’s correlation was used to separate 10893 assembled transcripts into 12 677 clusters (groups of coregulated genes). Gene lists derived from K-mean clusters were 678 analyzed for GO term enrichment. The cumulative probability (P value) of 679 hypergeometric distribution was calculated to evaluate the significance of the GO 680 enrichment from each K-mean clusters (Chien et al., 2015). Transcription factors 681 falling into the designated clusters were manually selected and verified by qRT-PCR 682 analysis (Fig. 3). 683 684 Phylogenetic tree construction 685 Protein sequences were aligned by ClustalW. The resulting alignments were used to 686 construct phylogenetic trees using MEGA 5.2.2 (Tamura et al., 2011). The 687 Maximum-likelihood method was used to generate phylogenetic trees and 1000 688 replicates were used for bootstrapping. Only bootstrap values of 50% or higher were 689 shown for each clade. The evolutionary distances were computed using the Poisson 690 correction method and the rate variation among sites was modeled with a gamma 691 distribution. 692 693 Plasmid construction and Arabidopsis transformation 694 Total RNA was isolated as previously described (Lin et al., 2014). Five micrograms 695 of total RNA was used for cDNA synthesis. LEC1 cDNAs from various plant species 696 (Zea maize, AF410176; Oryza sativa, AY264284; Glycine max, BD242763; 697 Arabidopsis thaliana, NM_102046; Brassica napa, EU371726) were aligned. The 698 evolutionarily conserved region of cDNA was used to design primer 5′-699 CACGCCAAGATCTCGGACGAC-3′ rapid amplification of cDNA ends PCR 700 (RACE-PCR) to isolate PaLEC1 cDNA. 3′ RACE-PCR was carried out using a 701 SMARTer RACE cDNA amplification kit according to the manufacturer’s 702 instructions (Clontech). The amplified PaLEC1 cDNA was verified by sequencing. A 703 new primer, 5′-TCAAGGAAGCTAAACATGCAA-3′, derived from the sequenced 704



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PaLEC1 cDNA was designed for 5′ RACE-PCR (SMARTer RACE cDNA 705 amplification kit, Clontech, USA). The full-length cDNA of PaLEC1 was BP 706 recombined into pDONRTM221 vector to make pDONR_PaLEC1. pDONR_PaLEC1 707 was then LR recombined with pK7WGF2 or pH7FWG2.0 (Karimi et al., 2002) to 708 make 35SCaMV:PaLEC1-eGFP or 35SCaMV:eGFP-PaLEC1 respectively. Similarly, 709 the full-length cDNA of PaSTM was PCR amplified and BP recombined into 710 pDONRTM221 vector to make pDONR_PaSTM. pDONR_PaSTM was then LR 711 recombined with pK2GW7.0, pK7WGF2.0, or pH7FWG2.0 to make 712 35SCaMV:PaSTM, 35SCaMV:eGFP-PaSTM, or 35SCaMV:PaSTM-eGFP 713 respectively. For PaBBM gene, the full-length cDNA of PaBBM was PCR amplified, 714 digested by XbaI and SalI, and cloned into a modified version of the pDONRTM221 715 vector (ccdB gene was replaced by multiple cloning sites from NotI to KpnI of 716 pBluescript vector) to make pDONR_PaBBM. pDOR_PaBBM was then LR 717 recombined with pH7FWG2.0 to make 35SCaMV:PaBBM-eGFP construct. 718 The resulting plasmids were transformed into Agrobacterium tumefaciens strain 719 GV3101. Wild-type strain (Wassilewskija ecotype) was transformed by A. 720 tumefaciens GV3101 using the floral dipping method (Clough and Bent, 1998). In 721 addition to antibiotic selection, the transformants were further verified by PCR 722 amplification of 207 bp DNA fragment using forward primer 5′-723 CACGCCAAGATCTCGGACGAC-3′ and reverse primer 5′-724 CTCACGGTATCGGTGGAGAT-3′ for PaLEC1; 525 bp DNA fragment using 725 forward primer 5′-GGAGGAGAGGATCCAGCTTT-3′ and reverse primer 5′-726 AAACTGCATCTCCTCCGATG-3′ for PaSTM; 279 bp DNA fragment using 727 forward primer 5′-TGTTGGAGAATGAGGGGAAG-3′ and reverse primer 5′-728 ATAAGCCCTTGCTGCCTTTT-3′ for PaBBM. For complementation test of 729 PaLEC1, 35SCaMV:PaLEC1-eGFP or 35SCaMV:eGFP-PaLEC1 was transformed 730 into the lec1-1 mutant (Lotan et al., 1998). 731 732 Quantitative RT-PCR 733 DNA-free RNA was reverse transcribed in the presence of a mixture of oligo dT 734 and random primers (9:1 ratio) using the GoScript Reverse Transcription System 735 (Promega) according to the manufacturer’s instructions. Ten microliters of RT-PCR 736 reaction contained 2.5 μl of 1/20 diluted cDNA, 0.2 μM of primers, and 5 μl of 2× 737 KAPA SYBR FAST master mix (KAPA Biosystems). The following program was 738



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used for amplification: 95°C for 1 min, 40 cycles at 95°C for 5 s and 58 to 62°C for 739 20 s (Supplemental Table S4). PCR was performed in triplicate, and the 740 experiments were repeated with RNA isolated from two independent samples. 741 Primer pairs and the specified annealing temperature used for quantitative PCR are 742 listed in Supplemental Table 5. Ubiquitin (PaUBI) was used as an internal control 743 (Lin et al., 2014). 744 745 In situ hybridization 746 Protocorms and PLB samples were fixed in 4% paraformaldehyde, 4% 747 dimethylsulfoxide, 0.25% glutaraldehyde, 0.1% Tween 20, and 0.1% Triton X-100 748 in diethylpyrocarbonate-treated H2O at 4°C overnight. Tissues were then dehydrated 749 and infiltrated with Paraplast (Leica) using a KOS Rapid Microwave Labstation 750 (Milestone). Tissues (10 μm thick) were sectioned using a MICROM 315R 751 microtome (Thermo Scientific) and mounted onto a poly-L-lysine-coated slide 752 (Matsunami). Sections were then de-paraffinized in xylene, rehydrated in decreasing 753 concentrations of ethanol, and digested with 2 mg/ml proteinase K at 37°C for 30 754 min. In situ hybridization was performed as previously described (Lin et al., 2014) 755 with hybridization temperature optimized for each gene: 62°C for PaBBM, 51.5°C 756 for PaLEC1, and 60°C for PaSTM. Tissue sections and in situ hybridization were 757 photographed on a Zeiss Axio Scope A1 microscope equipped with an AxioCam 758 HRc camera (Zeiss). 759 760 Sudan Red 7B staining 761 Sudan red staining has been described in detail (Harding et al., 2003). Briefly, 762 tissues were incubated in 70% (v/v) ethanol overnight to remove chlorophyll before 763 staining. Tissues were stained in 0.1% (w/v) Sudan Red 7B (Sigma) solution for 1 h 764 at room temperature, rinsed several times in water, and then mounted in glycerol for 765 examination under a SMZ800 stereoscopic zoom microscope (Nikon). 766 767 PaSTM antibody production 768 Specific antibody for PaSTM was generated in rabbits against a peptide region 769 (LHFHPRSKMENWSGGNNP) unique to PaSTM. This peptide was conjugated to 770 ovalbumin via a Cys residue and injected into rabbits according to the supplier’s 771 protocols (LTK BioLaboratories, Taiwan). The resulting antibody was affinity 772



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purified by column chromatography using PaSTM peptide. 773 774 Protein Isolation and Immunoblot Analysis 775 Approximately 0.1 g of tissues was homogenized in 1 ml of RIPA buffer (50 mM 776 Tris-HCl, pH 7.5, 150 mM NaCl, 1 mM EGTA, 0.25 (w/v) % deoxycholate, 0.1% 777 (w/v) SDS, and 1% (v/v) NP40) or 1 ml of Urea buffer (250 mM Tris-HCl, pH 6.8, 778 3.5% (w/v) SDS, 1 M Urea, and 10% (v/v) glycerol) supplemented with 1 mM 779 phenylmethanesulfonylfluoride, 1X protease inhibitor cocktail (Sigma) and 10 μM 780 MG132 (Sigma). Homogenized protein extracts were centrifuged at 16000 g at 4°C 781 for 5 min to remove cell debris. The protein concentration of the supernatant was 782 determined by DC Protein Assay Kit according to the manufacturer’s instructions 783 (Bio-Rad). Approximately 50 μg (PaLEC1 and PaBBM) or 100 μg (PaSTM) of 784 protein was resolved on a Bolt 4-12% or 10% Bis-Tris Plus gel (Invitrogen) and 785 transferred to Immobilon-P membrane (Millipore). Blots were blocked in 5% (w/v) 786 milk in Tris buffered saline solution with 0.1% (v/v) Tween 20. A 1:2000 dilution 787 of the GFP antibody (Roche) or purified PaSTM specific antibody was used as the 788 primary antibody. A 1:20000 dilution of horseradish peroxidase-conjugated anti-789 mouse IgG (Jackson ImmunoResearch Laboratories) or anti-rabbit IgG (Jackson 790 ImmunoResearch Laboratories) was used as the secondary antibody. The peroxidase 791 activity was detected by a chemiluminescence assay (Advansta). 792 793 Supplemental data 794 Supplemental Figure S1 A, Images of interior tissues of developing ovules harvested 795 at different stages for RNA-seq. B, K means clustering identified 12 groups of genes 796 associated with specific developmental stage. 797 Supplemental Figure S2 Phylogenetic relationship of MADS, AP2, HD-Zip, and B3 798 domain transcription factors. 799 800 Supplemental Figure S3 Protein sequence alignment of LEC1 and BBM proteins. 801 Supplemental Figure S4 Unrooted Maximum-likelihood trees of the 7S and 11/12S 802 albumins. 803 Supplemental Figure S5 Confirmation of PaLEC1-eGFP and PaBBM-eGFP protein in 804 overexpressor lines. 805



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Supplemental Figure S6 Phylogenetic relationship of Class-1 KNOX, AP2/ERF, and 806 WUS/WOX transcription factors. 807 Supplemental Figure S7 Overexpression of PaSTM causes abnormal meristems. 808 Supplemental Table S1 Statistics of the de novo transcriptome assembly. 809 Supplemental Table S2 Statistics of RNA-seq reads. 810 Supplemental Table S3 Statistics of twelve gene clusters in Supplemental Figure S1B. 811 Supplemental Dataset 1 Comparative transcript abundances of preferentially regulated 812 genes in reproductive tissues of P. aphrodite by RNA-seq analysis. 813 Supplemental Dataset 2 GO analysis of tissue-specific K-mean clusters. 814 Supplemental Dataset 3 Comparative transcript abundances of preferentially regulated 815 transcription factors in reproductive tissues of P. aphrodite by RNA-seq analysis. 816 817 ACKNOWLEDGMENTS 818 We express our appreciation to Dr. Donna Fernandez for providing the Arabidopsis 819 seeds, Dr. Swee-Suak Ko, Ms. Yi-Chen Lien, and Ms. Hue-Ting Yang for their 820 assistance with in situ hybridization, Miss Chi-Nga Chow and Dr. Wen-Chi Chang for 821 assistance with the GO analysis and comments on the manuscript, Mr. Cheng-Pu Wu 822 for database maintenance, AS-BCST Greenhouse Core Facility for greenhouse 823 service, and Ms. Miranda Loney for English editing. 824 Figure legends: 825 826 Figure 1. Fertilization-triggered reproductive program, protocorm, and PLB 827 development. A, Schematic diagram showing the timeline of reproductive 828 development in Phalaenopsis orchid. Images showing developing ovules or seeds in 829 developing ovaries collected at the specified day after pollination (DAP, 830 Supplemental Figure S1A). Red scale bar = 100 μm. The red asterisk “*” indicates the 831 developing ovule. The black asterisk “*” indicates the developing seed. Notice the 832 seed coat turns brown at 180 DAP. B, Images of developing protocorms at 10 days 833 (protocorm10), 20 days (protocorm20), or 30 days (protocorm30) after germination. 834 A, the anterior end of the protocorm; P, the posterior end of the protocorm. C, Images 835 of developing PLBs in small (PLBS), medium (PLBM), and large (PLBL) sizes. 836 Black or white scale bar = 1 mm. 837 838



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Figure 2. Protocorm and PLB are molecularly distinct from other reproductive tissues. 839 A, Principal component analysis of developing ovaries at 30-40 DAP, 50-60 DAP, 840 70-80 DAP, 90-100-120 DAP, 140-160 DAP, 180-200 DAP, PLBs, protocorms, 841 young leaves, stalk buds, and floral stalks. B, Heat map showing the P value 842 significance of enrichment of GO terms for stage-specific mRNAs. The empty cell 843 indicates lack of association. 844 845 Figure 3. Expression profiles of selected genes during reproductive development. A, 846 Expression patterns of transcription factors enriched in developing ovaries from 30 to 847 80 DAP. B, Expression patterns of genes enriched in developing ovaries from 100 to 848 200 DAP. Small sized PLB (PLBS), medium sized PLB (PLBM), large sized PLB 849 (PLBL), 10-day-old protocorms (protocorm10), 20-day-old protocorms 850 (protocorm20), and 30-day-old protocorms (protocorm30). 851 852 Figure 4. PaBBM and PaLEC1 mRNAs are present in developing embryos but not 853 PLB. A, In situ hybridization with an anti-sense (AS) PaBBM or PaLEC1 on 854 longitudinal sections through the center of the developing seeds at different days after 855 pollination (DAP). Sense probes (S) of PaBBM or PaLEC1 were used as a negative 856 control. E, embryo; white asterisk “*”, seed coat. B, In situ hybridization with anti-857 sense probe PaBBM-AS on longitudinal sections through the center of emerging 858 PLBs. C, In situ hybridization with anti-sense probe PaLEC1-AS on longitudinal 859 sections through the center of emerging PLBs. Black asterisk “*”, individual PLB. 860 Red scale bar = 20 μm. Blue scale bar = 200 μm. 861 862 Figure 5. PaBBM and PaLEC1 are sufficient to initiate somatic embryogenesis. A, 863 Overexpression of PaBBM-eGFP induces embryonic culture tissue (ECT) in wt. B, 864 Overexpression of eGFP-PaLEC1 induces ECT in wt. C, Expression of embryo-865 specific genes, CRU3, ABI3, and FUS3 in the ECT of PaBBM-eGFP overexpressors. 866 D, Expression of embryo-specific genes, CRU3, ABI3, and FUS3 in the ECT of 867 eGFP-PaLEC1 overexpressors. E, Sudan Red 7B staining indicates accumulation of 868 triacylglycerols in PaLEC1-eGFP and PaBBM-eGFP overexpressors. F, 869 Overexpression of eGFP-PaLEC1 rescues desiccation intolerance of Arabidopsis 870 lec1-1 mutant. The arrows indicate the complemented lec1-1 plants. CRU3, 871 Cruciferin 3; ABI3, Abscisic acid-insensitive 3; FUS3, Fusca 3. Scale bar = 500 μm. 872



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873 Figure 6. Expression of PaSTM mRNA is associated with PLB initiation. A, 874 Expression patterns of the indicated genes enriched in developing PLBs and/or 875 protocorms. B, Morphology of an explant, newly emerging PLBs (PLBN), and PLBS. 876 In situ hybridization with an anti-sense PaSTM on longitudinal sections through the 877 center of PLBN and PLBS. *, individual PLB. ca, callus tissues from which PLBs are 878 derived. C, In situ hybridization with an anti-sense PaSTM on longitudinal sections 879 through the center of protocorms. PaSTM-AS, antisense probe of PaSTM. PaSTM-S, 880 sense probe of PaSTM was used as a negative control. D, Expression patterns of the 881 indicated genes in callus, developing PLBs, and interior ovary tissues collected at 160 882 DAP (160 DAP). Small sized PLB (PLBS), medium sized PLB (PLBM), large sized 883 PLB (PLBL), 10-day-old protocorms (protocorm10), 20-day-old protocorms 884 (protocorm20), and 30-day-old protocorms (protocorm30). Scale bar = 200 μm. 885 886 Figure 7. Overexpression of PaSTM is capable to induce shoot regeneration program. 887 A, Overexpression of PaSTM was confirmed by immunobloting using a PaSTM-888 specific polyclonal antibody. The arrow indicates the full-length PaSTM protein. 889 Degraded PaSTM protein is marked by an asterisk. Protein loading was confirmed by 890 Ponceau S staining. B, Transgenic plant carrying the pK2GW7 vector. 891 Overexpression of PaSTM causes formation of (C) dome-shaped or (D) brush-like 892 shoot meristems, (E) lobed leaves, and (F) early bolting phenotypes. Red arrowheads 893 indicate the unorganized meristems. Red scale bar = 0.5 mm. G, Cauline and rosette 894 leaves of homozygous lines overexpressing PaSTM appeared to be curved and lobed. 895 Het, heterozygous line. Homo, homozygous line. White scale bar = 1 cm. H, 896 Transcript levels of RAP2.6L (At5g13330) and GA2OX2 (At1g30040) in wt and the 897 transgenic plants overexpressing PaSTM or carrying the empty pK2GW7 vector (V). 898 PaSTM (A), PaSTM overexpressors with abnormal seedlings. PaSTM (N), PaSTM 899 overexpressors with normal seedlings. DAG, day after germination. 900



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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Phylogeny and classification of the orchid family%2E%5BTitle%5D%29 AND Dressler RL%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Phylogeny and classification of the orchid family.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Trends Plant Sci%5BTitle%5D%29 AND 16%5BVolume%5D AND 597%5BPagination%5D AND Duclercq J%2C Sangwan%2DNorreel B%2C Catterou M%2C Sangwan RS%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 8%5BVolume%5D AND 155%5BPagination%5D AND Elliott RC%2C Betzner AS%2C Huttner E%2C Oakes MP%2C Tucker WQ%2C Gerentes D%2C Perez P%2C Smyth DR%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Elliott&as_ylo=1996&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell Tissue and Organ Culture%5BTitle%5D%29 AND 39%5BVolume%5D AND 273%5BPagination%5D AND Ernst R%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Effects of Thidiazuron on in-Vitro Propagation of Phalaenopsis and Doritaenopsis (Orchidaceae)&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://scholar.google.com/scholar?as_q=Evolution of asexual reproduction in leaves of the genus Kalancho�&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Garc�s&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

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Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo assembly of theArabidopsis shoot meristem. Development 134: 3539-3548


Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E,Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-lengthtranscriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29: 644-652


Harding EW, Tang W, Nichols KW, Fernandez DE, Perry SE (2003) Expression and maintenance of embryogenic potential isenhanced through constitutive expression of AGAMOUS-Like 15. Plant physiology 133: 653-663


Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt ED, Boutilier K, Grossniklaus U, de Vries SC (2001) The Arabidopsis SOMATICEMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogeniccompetence in culture. Plant physiology 127: 803-816


Hong PI, Chen JT, Chang WC (2008) Plant regeneration via protocorm-like body formation and shoot multiplication from seed-derived callus of a maudiae type slipper orchid. Acta Physiologiae Plantarum 30: 755-759


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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Curr Biol%5BTitle%5D%29 AND 12%5BVolume%5D AND 515%5BPagination%5D AND Golz JF%2C Keck EJ%2C Hudson A%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Spontaneous mutations in KNOX genes give rise to a novel floral structure in Antirrhinum&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Spontaneous mutations in KNOX genes give rise to a novel floral structure in Antirrhinum&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Golz&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Proc Natl Acad Sci U S A%5BTitle%5D%29 AND 106%5BVolume%5D AND 16529%5BPagination%5D AND Gordon SP%2C Chickarmane VS%2C Ohno C%2C Meyerowitz EM%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Gordon&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gordon&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Development%5BTitle%5D%29 AND 134%5BVolume%5D AND 3539%5BPagination%5D AND Gordon SP%2C Heisler MG%2C Reddy GV%2C Ohno C%2C Das P%2C Meyerowitz EM%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development 134: 3539-3548

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Gordon&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Pattern formation during de novo assembly of the Arabidopsis shoot meristem&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Pattern formation during de novo assembly of the Arabidopsis shoot meristem&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gordon&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nat Biotechnol%5BTitle%5D%29 AND 29%5BVolume%5D AND 644%5BPagination%5D AND Grabherr MG%2C Haas BJ%2C Yassour M%2C Levin JZ%2C Thompson DA%2C Amit I%2C Adiconis X%2C Fan L%2C Raychowdhury R%2C Zeng Q%2C Chen Z%2C Mauceli E%2C Hacohen N%2C Gnirke A%2C Rhind N%2C di Palma F%2C Birren BW%2C Nusbaum C%2C Lindblad%2DToh K%2C Friedman N%2C Regev A%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Grabherr&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Full-length transcriptome assembly from RNA-Seq data without a reference genome&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Full-length transcriptome assembly from RNA-Seq data without a reference genome&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Grabherr&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant physiology%5BTitle%5D%29 AND 133%5BVolume%5D AND 653%5BPagination%5D AND Harding EW%2C Tang W%2C Nichols KW%2C Fernandez DE%2C Perry SE%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Harding EW, Tang W, Nichols KW, Fernandez DE, Perry SE (2003) Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-Like 15. Plant physiology 133: 653-663

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http://scholar.google.com/scholar?as_q=Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-Like 15&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-Like 15&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Harding&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant physiology%5BTitle%5D%29 AND 127%5BVolume%5D AND 803%5BPagination%5D AND Hecht V%2C Vielle%2DCalzada JP%2C Hartog MV%2C Schmidt ED%2C Boutilier K%2C Grossniklaus U%2C de Vries SC%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt ED, Boutilier K, Grossniklaus U, de Vries SC (2001) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant physiology 127: 803-816

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hecht&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hecht&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Acta Physiologiae Plantarum%5BTitle%5D%29 AND 30%5BVolume%5D AND 755%5BPagination%5D AND Hong PI%2C Chen JT%2C Chang WC%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hong&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Plant regeneration via protocorm-like body formation and shoot multiplication from seed-derived callus of a maudiae type slipper orchid&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Plant regeneration via protocorm-like body formation and shoot multiplication from seed-derived callus of a maudiae type slipper orchid&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hong&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Bioinformatics%5BTitle%5D%29 AND 27%5BVolume%5D AND 3209%5BPagination%5D AND Howe EA%2C Sinha R%2C Schlauch D%2C Quackenbush J%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol%5BTitle%5D%29 AND 136%5BVolume%5D AND 3427%5BPagination%5D AND Hsieh K%2C Huang AH%5BAuthor%5D&dopt=abstract

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Kagaya Y, Okuda R, Ban A, Toyoshima R, Tsutsumida K, Usui H, Yamamoto A, Hattori T (2005) Indirect ABA-dependent regulationof seed storage protein genes by FUSCA3 transcription factor in Arabidopsis. Plant Cell Physiol 46: 300-311


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Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193-195


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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Curr Opin Plant Biol%5BTitle%5D%29 AND 15%5BVolume%5D AND 4%5BPagination%5D AND Jeong S%2C Volny M%2C Lukowitz W%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Jeong&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Axis formation in Arabidopsis - transcription factors tell their side of the story&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Methods Mol Biol%5BTitle%5D%29 AND 6%5BVolume%5D AND 181%5BPagination%5D AND Jones D%2C Tisserat B%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Jones D, Tisserat B (1990) Clonal propagation of orchids. Methods Mol Biol 6: 181-191

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Jones&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Clonal propagation of orchids&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Curr Biol%5BTitle%5D%29 AND 22%5BVolume%5D AND 1825%5BPagination%5D AND Jullien PE%2C Susaki D%2C Yelagandula R%2C Higashiyama T%2C Berger F%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Jullien PE, Susaki D, Yelagandula R, Higashiyama T, Berger F (2012) DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr Biol 22: 1825-1830

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Jullien&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Physiologia Plantarum%5BTitle%5D%29 AND 61%5BVolume%5D AND 377%5BPagination%5D AND Koornneef M%2C Reuling G%2C Karssen CM%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Orchid biology reviews and perspectives%2E%5BTitle%5D%29 AND Kull T%2C Arditti J%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kull T, Arditti J (2002) Orchid biology reviews and perspectives. Kluwer Academic Publishers., Dordrecht ; London

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kull&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Orchid biology reviews and perspectives.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nat Methods%5BTitle%5D%29 AND 9%5BVolume%5D AND 357%5BPagination%5D AND Langmead B%2C Salzberg SL%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Langmead&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Fast gapped-read alignment with Bowtie 2&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Fast gapped-read alignment with Bowtie 2&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Langmead&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%2869%2E The Biology of Myco%2DHeterotrophic %27Saprophytic%27 Plants%2E New Phytologist%5BTitle%5D%29 AND 127%5BVolume%5D AND 171%5BPagination%5D AND Leake JR%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Leake&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Tansley Review No&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://search.crossref.org/?page=1&rows=2&q=Lee Y-I, Yeung EC, Chung M-C (2007) Embryo Development of Orchids. World Scientific Publishing Co. Pte. Ltd., Singapore

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lee&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Embryo Development of Orchids.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Embryo Development of Orchids.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lee&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

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Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMCBioinformatics 12: 323


Lin CS, Hsu CT, Liao DC, Chang WJ, Chou ML, Huang YT, Chen JJ, Ko SS, Chan MT, Shih MC (2016) Transcriptome-wide analysisof the MADS-box gene family in the orchid Erycina pusilla. Plant Biotechnol J 14: 284-298


Lin HY, Chen JC, Wei MJ, Lien YC, Li HH, Ko SS, Liu ZH, Fang SC (2014) Genome-wide annotation, expression profiling, andprotein interaction studies of the core cell-cycle genes in Phalaenopsis aphrodite. Plant Mol Biol 84: 203-226


Lotan T, Ohto M, Yee KM, West MA, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFYCOTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93: 1195-1205


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Marhavy P, Bielach A, Abas L, Abuzeineh A, Duclercq J, Tanaka H, Parezova M, Petrasek J, Friml J, Kleine-Vehn J, Benkova E(2011) Cytokinin Modulates Endocytic Trafficking of PIN1 Auxin Efflux Carrier to Control Plant Organogenesis. Developmental cell21: 796-804


Marhavy P, Duclercq J, Weller B, Feraru E, Bielach A, Offringa R, Friml J, Schwechheimer C, Murphy A, Benkova E (2014) Cytokinincontrols polarity of PIN1-dependent auxin transport during lateral root organogenesis. Curr Biol 24: 1031-1037


Masiero S, Colombo L, Grini PE, Schnittger A, Kater MM (2011) The emerging importance of type I MADS box transcription factorsfor plant reproduction. Plant Cell 23: 865-872


Maximova SN, Florez S, Shen X, Niemenak N, Zhang Y, Curtis W, Guiltinan MJ (2014) Genome-wide analysis reveals divergentpatterns of gene expression during zygotic and somatic embryo maturation of Theobroma cacao L., the chocolate tree. BMC PlantBiol 14: 185


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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Development%5BTitle%5D%29 AND 129%5BVolume%5D AND 3195%5BPagination%5D AND Lenhard M%2C J�rgens G%2C Laux T%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Genome%2Dwide analysis reveals divergent patterns of gene expression during zygotic and somatic embryo maturation of Theobroma cacao L%2E%2C the chocolate tree%2E%5BTitle%5D%29 AND Maximova SN%2C Florez S%2C Shen X%2C Niemenak N%2C Zhang Y%2C Curtis W%2C Guiltinan MJ%5BAuthor%5D&dopt=abstract

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Zhang GQ, Xu Q, Bian C, Tsai WC, Yeh CM, Liu KW, Yoshida K, Zhang LS, Chang SB, Chen F, Shi Y, Su YY, Zhang YQ, Chen LJ,Yin Y, Lin M, Huang H, Deng H, Wang ZW, Zhu SL, Zhao X, Deng C, Niu SC, Huang J, Wang M, Liu GH, Yang HJ, Xiao XJ, Hsiao YY,Wu WL, Chen YY, Mitsuda N, Ohme-Takagi M, Luo YB, Van de Peer Y, Liu ZJ (2016) The Dendrobium catenatum Lindl. genomesequence provides insights into polysaccharide synthase, floral development and adaptive evolution. Sci Rep 6: 19029


Zhao P, Wu F, Feng F-S, Wang W-J (2008) Protocorm-like body (PLB) formation and plant regeneration from the callus culture ofDendrobium candidum Wall ex Lindl. In Vitro Cellular & Developmental Biology 44: 178-185


Zhao Y, Tang H, Ye Y (2012) RAPSearch2: a fast and memory-efficient protein similarity search tool for next-generation sequencingdata. Bioinformatics 28: 125-126



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