Oil Palm Bulletin 43 p. 1-13 Genes Controlling Flowering ...palmoilis.mpob.gov.my/publications/OPB/opb43-sharifah.pdf · Genes Controlling Flowering: Possible Roles in Oil Palm Floral

Genes Controlling Flowering: Possible Roles in Oil Palm Floral Abnormality

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Genes Controlling Flowering: Possible Roles in OilPalm Floral Abnormality

Sharifah Shahrul Rabiah Syed Alwee*

* Malaysian Palm Oil Board, P.O. Box 10620, 50720 Kuala Lumpur, Malaysia.

ABSTRACT

Floral abnormality in clonal oil palm results inbunch failure and a reduction of oil yield. Anin-depth study of oil palm flower development isimportant to understand the factors involved inthis phenomenon. Based on the success of flowerdevelopment studies of Arabidopsis and rice,efforts have been directed at investigating oilpalm flower development. Numerous genes havebeen cloned and their putative functions stud-ied. Changes in the expression level of somehomeotic genes have been detected in abnormalflowers and meristem. Efforts are currently be-ing made to correlate these changes to a meas-urable physical characteristic to assist inmarker development.

ABSTRAK

Abnormaliti bunga sawit menyebabkanpembentukan buah yang tidak sempurna danpenurunan hasil minyak sawit. Suatu kajianyang mendalam terhadap pembentukan bungasawit adalah penting bagi memahami faktor-faktor yang terlibat di dalam fenomena ini.Berdasarkan kejayaan kajian pembentukanbunga Arabidopsis dan padi, usaha-usahatelah dijalankan bagi mengkaji pembentukanbunga sawit. Pelbagai gen telah pun diklonkandan fungsi-fungsinya dikaji. Perubahan padatahap ekspresi beberapa gen homeotik telahdapat dikesan di dalam bunga abnormal danmeristemnya. Kajian bagi mengaitkanperubahan ekspresi gen ini kepada sesuatu cirifizikal yang dapat diukur sedang dilakukan.Ini akan dapat membantu di dalampembentukan penanda bagi pengesanan awalabnormaliti bunga sawit.

INTRODUCTION

The commercial exploitation of tissue culturewas hampered when floral and fruitabnormalities were reported in clonal plantings(Corley et al., 1986). In an abnormal maleinflorescence, some or all the individual maleflowers develop as females and the normalsessile androecium develops into a stigma-likestructure (feminization). In some cases, smallfruitlets develop. In the abnormal femaleinflorescence, mantled fruits develop. Thesefruits have a ring of six appendages known assupplementary carpels. A high proportion ofthese abnormal fruits fail to ripen and often rotbefore oil synthesis occurs. This abnormality hasbeen reported to be expressed irregularly withinand between bunches in many abnormal ramets.Sometimes only some flowers within a bunch areabnormal while the rest remain normal.

Many studies on the phenomenon of floralabnormality have been carried out and severalpossible causes have been reported (Sharifah andCheah, 2001). However, to date, there is no con-clusive evidence on the actual cause of the ab-normality.

During the past decade, tremendousprogress has been made in understanding themolecular mechanisms of flower development indicots and monocots. Most of the molecular andgenetic information has been available from re-search conducted in Arabidopsis and Antirrhi-num. Using these studies as guidance, oil palmflower development was examined to shed somelight on the possible causes and solutions to thefloral abnormality problem. This approach wastaken since the floral abnormality is due to anaberration in the developmental steps during oilpalm flower development. Flower developmentalstudy will also provide an understanding of thebiology of the oil palm production processes. Thisunderstanding will allow us to exploit the physi-ology of the oil palm for better crop production.This paper aims to provide an insight in to thesteps leading to flower formation from a molecu-lar biology point of view and how these stepsmight affect oil palm flowering leading to themantled floral abnormality.

Keywords: oil palm, flower development,MADS-box genes, floral abnormality, floweringpathways.

Oil Palm Bulletin 43 p. 1-13

Oil Palm Bulletin 43

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THE STEPS OF FLOWER DEVELOPMENT

Plants have two basic growth modes during theirlife cycle � vegetative and reproductive growth.The shoot apical meristem (SAM) is responsiblefor the growth of all vegetative parts of a plant.SAM is initially formed during embryogenesiswhen the basic body architecture of a plant isestablished (Jurgens, 1995). SAM generatesstems, leaves and floral organs in a set patternwhile it maintains a pool of undifferentiated cellsin the centre (Steeves and Sussex, 1989). Thus,SAM formation during embryogenesis is acritical step to subsequent vegetative andreproductive development.

The main functions of SAM are to: (i)initiate the formation of lateral organs andstructures (e.g. leaves and flowers); and (ii)maintain a population of undifferentiated cellsthat remains uncommitted. This ability toremain uncommitted allows the plant greatflexibility in its developmental programmes. TheSAM switches to reproductive growth (flowering)when it receives the appropriate signals. Thisswitch is tightly controlled by numerousphysiological signals and genetic pathways thatcoordinate flowering with environmentalconditions and the developmental stage of theplant (Bernier, 1988; Levy and Dean, 1998). Thisswitch is a pivotal event in a plant�s life. Whenthis occurs, a cascade of processes is triggeredwithin SAM resulting in its restructuring andformation of floral structures. The signals thatregulate the transition to flowering originateoutside SAM. For both environmentallyresponsive and autonomous plants, the signalsprobably originate in the leaves (Bernier et al.,1993; Lang, 1977).

Once the meristem is triggered to producea flower, the type, number and position of theorgans constituting the flower are strictlyregulated. The floral meristems will undergo aseries of developmental changes that eventuallygive rise to the four basic floral structures �sepals, petals, stamens and carpels (Figure 1).The sepals, forming the outermost whorl, aremost similar to leaves. The petals on the secondwhorl are often brightly coloured to attractinsects for pollination. Stamens, which are insidethe petals, carry the pollen grains and thecarpels in the central whorl, carry the ovules. Inthe oil palm, both male and female flowers havetwo whorls of perianths followed by rudimentarystamens for female flowers or androecium for themale flowers. The central whorl carries therudimentary gynoecium for male flowers orcarpels for female flowers. The carpels will later

give rise to the fruits.

GENES INVOLVED INFLOWER DEVELOPMENT

The process of flower development can besubdivided into four steps, with each stepaffected by different genes (Figure 2) (Weigel andMeyerowitz, 1994; Ma, 1994). The first step isfloral induction, resulting in conversion of thevegetative meristem to an inflorescencemeristem. The floral induction process is affectedby more than 10 flowering genes and mutationsin these genes accelerate or delay flowering(Koorneef et al., 1998).

The second step is the development of theflower meristem through distinct pattern of celldivisions in the inflorescence meristem. Thegenes that control floral meristem formation arecalled meristem identity genes. FLORICAULA(FLO) and SQUAMOSA (SQUA) in Antirrhinumand LEAFY (LFY) and APETALA1 (AP1) inArabidopsis are floral meristem identity genesthat have been studied extensively (Coen andCarpenter, 1993; Coen et al., 1990; Huijser et al.,1992; Weigel et al., 1992). LFY and AP1 aremaster regulators that mark primordialmeristematic cells for a floral fate (Pidkowich etal., 1999). On the other hand, TERMINALFLOWER 1 (TFL1) plays a major role inmaintaining the vegetative identity ininflorescence meristem (Alvarez et al., 1992). Abalance between the actions of LFY/AP1 andTFL1 is needed for a plant to produce flowersand yet continue producing leaves during its lifecycle.

The third step in flower development is theformation of flower organ primordia from thefloral meristem. Genes related to the formationof flower organ primordia are called cadastralgenes. Cadastral gene mutations affect floralorgan development differently depending on thetype of genes. Mutations in the clavata 1 geneaffect the number of carpels and other floralstructures without affecting the morphology ofthe structures (Clark et al., 1993). Othercadastral genes have been found to limit theexpression of certain target genes to certaindomains (Gaiser et al., 1995).

The final stage of flower development isthe determination of the organ primordia andtheir subsequent differentiation into organsappropriate to their positions. This process is con-trolled by organ identity genes. They can also influencemeristem determinacy as well as affect the organ type.


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Figure 1. Comparison between rice, Arabidopsis and oil palm flowers. Green, purple, yellow andred represent the four common flower organs, i.e. sepal, petal, stamen and carpel, respectively.

Figure 2. Four major steps of flower development.

ArabidopsisRice

Oil Palm female Oil Palm male


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AGAMOUS (AG), which encodes MADS-domain tran-scription factors, is best known for this role as well asspecifying reproductive organ identity (Yanofsky et al.,1990). These groups of genes will be further discussedin the following topic.

THE ABC OF FLOWER DEVELOPMENT

Flower development studies in Arabidopsis andAntirrhinum have led to development of a modelto explain the interactions of the different genesthat control the development of the various floralstructures (Coen and Meyerowitz, 1991). Themodel is known as the ABC model as all of thegenes involved can be classified as expressingone of three activities, A, B or C. This simplemodel provides a conceptual framework forexplaining the activities of the ABC genesleading to the production of four organ types ofthe typical flower. On this aspect, how oil palmflower development fits into the ABC model isstill unknown as oil palm flowers do not have thetypical sepal-petal-stamens-carpel structure.However, research on other monocots such asmaize has revealed that the ABC model is indeedcharacteristic of most angiosperms (Ambrose etal., 2000).

Mutations in the ABC organ identity geneslead to homeotic conversions of organ types,indicating that the ABC genes specify the fate offloral organ primordia (Coen and Meyerowitz,1991; Schwarz-Sommer et al., 1990; Bowman etal., 1991). The ABC genes act alone or incombination to specify the four flower organtypes. The A gene activities control thedevelopment of the sepal and petal, B geneactivities control petal and stamen developmentand C gene activities control stamen and carpeldevelopment. Figure 3 summarizes theseinteractions.

In general, if an A function gene ismutated, the first whorl develops as a carpel andthe second whorl as a stamen. The mutation ofB function gene would result in the developmentof sepals rather than petals in whorl 2, andcarpels and not stamens in whorl 3. Finally, Cfunction gene mutants have the third whorldevelop into a new flower with the sepal-petal-petal pattern. Table 1 summarizes thephenotypic effects of these mutations.

The A, B, and C genes are part of a groupof genes known as homeotic genes because theyare involved in the spatial arrangement of cells and tis-sues within the organism. Mutations in these genes re-sult in the transformation of one floral organ type to

another. In recent years, a series of these genes havebeen identified and isolated in various plants. To date,one A function gene, two B function genes and one Cfunction gene have been identified in Arabidopsis.They are APETALA2 (AP2), APETALA3 (AP3),PISTILLATA (PI) and AGAMOUS (AG), respectively(Irish and Sussex, 1990; Mandel et al., 1992; Jack etal., 1992; Goto and Meyerowitz, 1994; Yanofsky et al.,1990). Figure 4 show the images of wild-type andmutant Arabidopsis defective in their A, B or C genes.

These genes represent a single family ofDNA-binding transcriptional regulators, encodedby the MADS-box genes. They act as transcrip-tion factors, suggesting that the developmentalprocess resulted from a transcriptionally regu-lated cascade. This simply means that eventhough these genes control the development offloral organs, they themselves are being regu-lated by other genes. Studies have shown thatregulators of organ identity genes are the genesthat control the earlier steps of flower develop-ment including cadastral genes and meristemidentity genes.

In addition to the ABC genes, otherMADS-box genes also contribute their activity.These include APETALA2 (AP2), which preventsthe accumulation of AG RNA in the two outerwhorls (sepals and petals) (Drews et al., 1991;Jofuku et al., 1994). Recently, SEPALLATA 1/2/3 (SEP 1/2/3) was found to be another class oforgan-identity genes required for thedevelopment of petals, stamens and carpels(Pelaz et al., 2000).

MADS-BOX GENES

Molecular analysis has demonstrated that mostof the floral homeotic genes isolated to date be-long to the MADS-box regulatory gene family.The term MADS is derived from the first lettersof the genes MCM1, AGAMOUS, DEFICIENSand SRF. MCM1 and SRF are transcription fac-tors of yeast and human, respectively, whileAGAMOUS and DEFICIENS are among the firstof such genes isolated from plants. All of thesegenes have been shown to have similar structureto other MADS-box genes from plants. Each ofthese genes contains a 56-amino acid sequence(MADS) that is necessary for protein to bind toDNA. Plant MADS-box genes contain a secondconserved sequence called the K-domain becauseit is similar to the coiled-coil domain of keratin.This region has been implicated in the interaction ofproteins (Shore and Sharrocks, 1995). Figure 5 showsthe general structure of MADS-box genes.


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Figure 3. A summary of the arrangement and interaction of the A, B and C genes.

TABLE 1. PHENOTYPIC EFFECTS OF MUTATIONS IN A, B, OR C FUNCTIONORGAN IDENTITY GENES

Mutat ion Whorl 1 Whorl 2 Whorl 3 Whorl 4 G e n e s

Wildtype Sepal Pe ta l S tamen Carpel �

A function Carpel S tamen Stamen Carpel AP2

B function Sepal Sepal Carpel Carpel A P 3 / P I

C function Sepal Peta l Peta l New flower A G

The highly conserved MADS-domain is the ma-jor determinant of DNA-binding, but it also performsdimerization and accessory factor binding functions.The relatively weakly conserved I-domain may consti-tute a key molecular determinant for the selective for-mation of DNA-binding dimers (Reichmann andMeyerowitz, 1997). The K-domain is defined by a con-served regular spacing of hydrophobic residues, whichis proposed to allow for the formation of anamphiphatic helix involved in protein dimerization(Reichmann and Meyerowitz, 1997). The very variableC-domain at the C-terminus of the MADS-domain pro-teins is involved in transcriptional activation, or theformation of multimeric transcription factor com-plexes (Egea-Cortines et al., 1999).

Plant MADS-box genes constitute a hugemultigene family whose members control diversedevelopmental processes ranging from root toflower and fruit development. To date, there are44 distinct sequences of MADS-box genes inArabidopsis (Purugganan et al., 1995; Alvarez-Buylla et al., 2000b). Most plant MADS-boxgenes are expressed in flower tissues and areinvolved in the different phases of flower devel-opment (Weigel and Meyerowitz, 1994; Reichmann andMeyerowitz, 1997). The importance of MADS-boxgenes cannot be overemphasized as they controlflowering time, meristem identity and organ identity. Assuch, they are also known as molecular architects offlower morphogenesis.

Whorl 1 2 3 4

B

A C

1 2 3 4

B

C

Organ s e p e s t c a

Wildtype

c a s t s t c a

A mutantapetala2

Whorl 1 2 3 4

A C

1 2 3 4

B

Organ s e s e c a c a s e p e p e f

B mutantapetala3/pistillata

A

C mutantagamous


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Figure 4. Wildtype Arabidopsis and mutants of the organ identity genes.

Figure 5. A general structure of MADS�box genes.

Source: Dr Martin Yanofsky Lab Homepage at www.biology.ucsd.edu

CK BoxlMADSN

Wildtype apetala1 mutant

apetala2 mutant

agamous mutant

apetala3 mutant


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In recent years, studies on MADS-box genefunction have gone far beyond meristem identityand organ identity genes of model plants. Simi-lar genes have now been studied in other dicotsand monocots including oil palm. These studieshave concluded that flower development in bothdicots and monocots is based on highly conservednetworks of developmentally-controlled factors.

There is increasing evidence to suggestthat a large number of plant MADS-box geneshave functions that deviate from those of thetypical meristem identity and organ identitygenes (Alvarez-Buylla et al., 2000a). Their ex-pression has been found also in vegetative tis-sues, ovules, trichomes, roots, guard cells,endosperm, pollen and embryos (Colombo et al.,1995; Ma et al., 1991; Rounsley et al., 1995;Zhang and Forde, 1998; Alvarez-Buylla et al.,2000a). This observation further suggests thatthis family of genes play diverse roles through-out plant development. The expression patternsof some genes (e.g. FBP2 and TM5) also suggestthat they act as mediators between meristemidentity and organ identity genes (Angenent etal., 1994).

CLONING OF FLOWERING GENESFROM OIL PALM

Cloning of oil palm genes involved in floweringhas been achieved mainly by heterologous prob-ing with other MADS-box genes, PCR amplifica-tion, cold-plaque hybridization, differentialscreening and subtractive hybridization. Cur-rently, we have isolated nine MADS-box genes,two meristem identity genes, four flowering timegenes and numerous other flowering genes.

The availability of molecular probes forregulatory genes is useful as it permits the studyof the expression of these genes in tissues andcells giving rise to the flowers. Typically,northern hybridizations are used to study geneexpression. Figure 6 shows an example of anorthern hybridization result. In this case, thenorthern blot carries total RNA from variousstages of flowering from both normal andabnormal palms of the same clone. This blot ishybridized or probed with an oil palm homologueof AP1, a meristem identity gene. The hybridizationsignals obtained indicated that there is a significant re-duction in expression level of OPAP1 in abnormalflowers. This suggests that meristem development isaffected during the flowering process of abnormalpalms.

Sometimes, due to the structure of the oil palm

flower, this technique does not give an accurate expres-sion pattern of the gene of interest. This is because, foraccuracy, northerns require the isolation of mRNAfrom specific tissues in which the genes are expressed.These would be either carpels, stamens, bracts, pollensor even meristem cells. Separation of these organs isvery difficult for small flowers such as those of the oilpalm. Moreover, many of the floral regulatory genescloned are transcriptionally regulated such that theirRNAs accumulate in specific regions of early develop-ing flowers. Thus, in situ RNA hybridization is an alter-native procedure to study cell specific expression. Withthis procedure, a tissue section is probed with a labelledRNA probe. If the target RNA is present, a hybridizationsignal will be detected. Figure 7 shows some of theexpression patterns of oil palm flowering genes in oilpalm floral cells and tissues. In situ RNA hybridizationwith these molecular probes may also serve as an indi-cator of developmental zones within reproductive struc-tures thus allowing a comparison between the structuralunits in different flowers or reproductive tissues.

Other molecular genetic tools may helpelucidate functions of genes isolated. Genes canbe transformed in Arabidopsis to determine theireffects and to detect conservation of function.Several oil palm flowering genes have beentransformed currently for this purpose (Figure8).

FLOWER DEVELOPMENTAL ABERRATIONLEADING TO FLORAL ABNORMALITIES

Flower development is determined by a complexnetwork of regulators that control the formationof the inflorescence meristem and its transitionto the floral meristem, the initiation of floralorgan primordia and the floral organ identities.Figure 9 shows a flower developmental pathwaythat has been deduced for Arabidopsis (Blazquez,2000). This diagram displays the most currentknowledge of the pathways that are involved indetermination of flower architecture. In thispathway, environmental signals triggerflowering time genes that start reproductivedevelopment by activating meristem identitygenes. Environmental signals that play major roles areday length, hormones, sucrose level and temperature.Meristem identity genes control the transition frominflorescence to floral meristems. Cadastral genes setthe boundaries of floral homeotic gene function. Thehomeotic organ identity genes specify the organ iden-tity within the flower by activating downstream genes,which are direct or indirect targets of the organ identitygenes. Most genes involved regulate each other at thetranscriptional level, constituting a gene network. Someof the genes in this network have been isolated from oilpalm. We need to study them properly to determine the


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Figure 6. Northern hybridization using oil palm homologue of AP1 as probe, Blot A carries totalRNA of inflorescence from a normal palm of clone P75 and Blot B carries total RNA of inflores-

cence from an abnormal palm of the same clone. On Blot A, 1-vegetative meristem; 2-inflorescencemeristem; 3-flower meristem, 4-1.5 cm female infl.; 5-2 cm male infl.; 6-25 cm male infl.;

7-4 cm male infl.; 8-5 cm male infl.; 9-6 cm male infl.; 10-12 cm male infl.; 11-19 cm male infl.;12-27 cm male infl.; 13-34 cm male infl. On Blot B, 1-vegetative meristem; 2-flower meristem;3-1.5 cm female infl.; 4-2 cm female infl.; 5-35 cm female infl.; 6-5 cm female infl.; 7-11 cm

female infl.; 8-18 cm female infl.; 9-29 cm female infl.; 10-35 cm female infl.

Figure 7. Expression of oil palm homologues of Skp1 (A) and LEAFY (B) indicating thatexpression of these genes is localized to dividing cells in flower meristem and pollen of

abnormal flowers, respectively.

A

1 2 3 4 5 6 7 8 9 10 11 12 13

B

1 2 3 4 5 6 7 8 9 10

A B


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Figure 8. Transgenic Arabidopsis with 35S OPSOC1(oil palm homologue of SOC1, a flowering time gene).

Figure 9. Flower developmental pathways.

Source: Blazquez (2000).

Transgenic Transgenic Wildtype


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pathways at which the aberration takes place leading tofloral abnormality. Perhaps, the hormone-dependentpathway and sucrose-dependent pathway are importantfor oil palm as these two factors have been implicatedin one way or another in oil palm floral abnormality.

Loss of function of AP3 and PI (B-typegenes) results in phenotypic alterationsreminiscent of those observed in mantled flowersof the oil palm (Figure 3). This resemblance hasprompted investigation of whether theexpression of these genes is affected duringmantling. Preliminary investigation indicatesthat the transcript level of these genes inabnormal flowers of the oil palm is reducedsignificantly when compared with the leveldetected with normal flowers (unpublished).These genes, however, are transcription factorsinteracting with each other and/or with otherfactors in regulatory functions (Schwarz-Sommeret al., 1990; Trobner et al., 1992). This meansthat alone, it cannot confer the abnormalityphenotype. Other factors and genes need to comeinto play. The most immediate genes thatinteract with AP3 and PI are the meristemidentity genes that function as activators of AP3and PI (Weigel and Meyerowitz, 1993). We havecloned these genes, namely, OPLFY (an oil palmhomologue of LEAFY) and OPAP1 (oil palmhomologue of APETALA1) and shown that theirexpression is also affected in abnormal flowerssuggesting that meristem identity is alsoaffected in abnormal palm (Figure 6). However,more genes must be interacting with the B-typegenes and thus we have embarked on a yeast-two hybrid assay to isolate the interactingproteins in both normal and abnormal oil palmflowers.

The functions of meristem identity genesare highly regulated by flowering time genes.Among the many flowering time genes, we havecloned the oil palm homologues of CONSTANS(CO), Suppressor of Constans 1 (SOC1) andCircadian Clock Associated 1 (CCA1). Analysis of theexpression pattern of the oil palm homologue of SOC1(OPSOC1) indicates that it is expressed in most tissuesin oil palm and its expression is not significantly af-fected in abnormal palms.

We also have initiated work to isolate the targetsof organ identity genes. This will help us understand theway organ identity is realized during flower develop-ment. Several DNA binding proteins have also been iso-lated and are currently being studied in normal and ab-normal palms.

By now, it should be realized that the genenetworks controlling flower development are not exclu-

sively composed of MADS-box genes. Knowledge onthe number, type and interactions of the genes consti-tuting the network is still incomplete. However, thisgene network and regulators provide many differenttargets for mutational changes which vary greatly intheir phenotypic outcome. The mutational changes mayalso affect the structure of the proteins. Changes in thecis-regulatory or trans-regulatory elements of a genecould also occur. Amino acid changes in a transcriptionfactor might lead to numerous yet coordinated changesin downstream gene activation.

Currently, our experimental data indicatethat step 2 and step 4 (Figure 2) are affectedduring the development of abnormal flowers. Wenow need to find out why and how they areaffected. We also need to study if theabnormality also affects the cadastral genes andthe targets of the organ identity genes. Our aimis to correlate the changes in gene expressionthat occur with the physiological state of thepalm and cultures, such as content ofendogenous phytohormones, and methylationpattern changes occurring during tissue cultureand flower development. The answers to thesequestions can perhaps help us formulateprogrammes for early detection of the problem.

CONCLUSION

The recent availability of oil palm homologues ofkey players of the flower development genenetwork presents several novel opportunities foraddressing the question relating to floralabnormality. The more immediate goal of thisstudy is to correlate the changes in geneexpression leading to floral abnormality withmeasurable physiological changes occurring inthe plant or culture. This will not be an easytask. However, with the availability of tools tostudy flower development in oil palm and knowledge ofthe process, we may now have a chance to see the fullpicture.

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Oil Palm Bulletin 43 p. 1-13 Genes Controlling Flowering ...palmoilis.mpob.gov.my/publications/OPB/opb43-sharifah.pdf · Genes Controlling Flowering: Possible Roles in Oil Palm Floral