Bot. J. Linn. SOC., 62, pp . 77-84. With I plate

The occurrence of nitrogen-fixing root nodules on non -leguminous plants

C. RODRIGUEZ-BARRUECO Department of Botany, University of Glasgcrur" Accepted for publication April 1968

At present it is known that some 13 genera of non-leguminous Angiosperms include at least some species which bear root nodules with the property of nitrogen fixation. Alnus is the best known example. To assist in the assessment of the ecological importance of these plants, the author has surveyed the relevant literature to discover how many species in each of the genera have been recorded to bear nodules. He also provides evidence of this feature in several species not hitherto reported. Of an estimated total complement of 342 species in the 13 genera, 118 species have so far been recorded to bear nodules. The remaining species do not appear to have been examined for the presence of nodules.

CONTENTS

Introduction . . 77 Records of nodulated species . . 78 Discussion . . 81 Acknowledgements . * 82 References . . . . 82

PAGE

INTRODUCTION

Two types of nitrogen-fixing root nodules are found in the Angiosperms, firstly those inhabited by rhizobia present on most leguminous plants, and secondly those occurring on a much less closely interrelated group of plants, all woody, of which AZnus spp. are the best-known members, The nodule on these non-leguminous plants begins as a somewhat tuberous lateral root, which by repeated, close-set branching produces a coralline, perennial nodule-cluster which may eventually attain an over-all diameter of several centimetres. Plate 1A shows early stages in the formation of such nodule- clusters in Ceanothus. Internally the structure of each lobe of the cluster is that of a slightly modified root, of which the swollen cortex houses an endophyte; no confirmed isolation of any of the endophytes has been achieved, but on the basis of light- and electron-microscope studies of nodule sections it is widely believed that the endophytes are Actinomycetes. The morphology, physiology and biochemistry of these non- leguminous nodules have been fully reviewed by Allen & Allen (1965), Bond (1963, 1967) and Becking (1966). The benefit which the presence of nodules can confer on the plant is indicated in Plate 1B.

* Now at Instituto de Edafologia y Agrobiologia, Universidad de Salamanca, Espaiia.

78 C . RODRIGUEZ-BARRUECO

RECORDS OF NODULATED SPECIES

Present evidence suggests that nodules of this type occur on at least some species of 13 genera which are listed in Table 1, though for some of the genera, particularly Arctostaphylor, knowledge of the nodules is as yet insufficient to permit certainty that in structure and physiology they resemble the Ahus type. It is clear from Table 1 that, although some of the genera are closely related, collectively they form a very heterogen- eous group.

Table 1. Non-leguminous genera with nodule-bearing species, and their classification according to Engler (1964)

Genus Family Order

Casuarina Adans. MyVica L. Ahus Mill. Dryas L. Cercocarpus Kunth Purshia DC. Coriauiu Hook. Ceanothus L. Discaria Hook. Elaeagnus L. Hippophac)' L. Shepherdia Nutt. Arctostaphylos Adans.

Casuarinaceae Myricaceae Betulaceae Rosaceae (tribe Dryadeae) Rosaceae (tribe Dryadeae) Rosaceae (tribe Dryadeae) Coriariaceae Rhamnaceae Rhamnaceae Elaeagnaceae Elaeagnaceae Elaeagnaceae Ericaceae

Verticillatae Juglandales Fagales Rosales Rosales Rosales Sapindales Rhamnales Rhamnales Thymelaeales Thymelaeales Thymelaeales Ericales

Evidence is accumulating that these plants are important ecologically as providers of fixed nitrogen for other plants, as is, for example, indicated by the work of Lawrence and his associates (Crocker & Major, 1955 ; Lawrence et al., 1967) on the role of Alnus crispa (Ait.) Pursh. and Dryas drummondii Richardson in recently deglaciated areas of Alaska, and by the demonstration by Goldman (1961) of the contribution by AZnus tenuifolia Nutt. to the fertility of lake water in California.

For the assessment of the general biogeochemical significance of these plants it is obviously important to know whether the possession of nodules is common to all species of the genera listed in Table 1. Records of nodulation in these plants are scattered through papers of very varied types, and the task of compiling a complete list has rarely been attempted. Allen & Allen (1958) provided a list of some 54 species recorded as bearing nodules and later (Allen & Allen, 1965) extended this to 99 species. Meanwhile a need for an up-to-date list had arisen in connection with a proposed survey of non- leguminous nodulated plants under the International Biological Programme, and in 1964 the writer commenced to compile such a list at Professor G. Bond's suggestion. By further research in the literature and by including records which have become available in the last two years, it has been possible to increase the total of recorded species substantially, while for certain species earlier records than those cited by Allen & Allen have been traced. Since the second list by these authors appeared in a publica- tion which may not be generally available, it seemed more useful to provide a revised complete list rather than a series of amendments to their list,

ROOT NODULES ON NON-LEGUMINOUS PLANTS

Table 2. Non-leguminous Angiosperms reported to bear Alnus-type root nodules

79

ALNUS A. glutinosa (L.) Gaertn. (Meyen, 1829); A. glutinosa (L.) Gaertn. var. subbarbata, A. incana (L.) Moench (Woronin, 1866); A. undulata Willd. (Brunchorst, 1886-8); A. incana (L.) Moench var. glauca Ait. (Shibata, 1902); A. crispa(Ait.) Pursh (Kellerman, 1911); A. firma Sieb. & Zucc., A. japonica Sieb. &Zucc. (ShibatakTahara, 1917); A. fmmosanaMak. (Wilson, 1920-2); A. nitidaEnd1. (Parker, 1932); A.frzcticosa Rupr. (Rabotnov & Mednis, 1936); A. mollis Fernald (Bushnell& Sarles, 1937); A. cordata (Lois.) Desf., A. viridis Regel (Roberg, 1938); A. jorullensis Kunth var. spachii (Regel) Kunth (Castel- lanos, 1944); A. multinervis Matsum., A. sieboldiana Matsum., A. tinctoria Sarg. var. glabra Call. (Uemura, 1952~); A. mritima Nutt. (Uemura, 19523); A. hirsuta Turcz. (Karavayev, 1959); A. sinuata Rydb. (Furman, 1959); A. rubra Bongard (Tarrant, 1961); A. tenuifolia Nutt. (Goldman, 1961); A. nepalensis D. Don, A. orientalis Dcne (Uemura, 1964); A. rugosa (Du Roi) Spreng. (Moore, 1964); A. jorullensis Kunth", A. serrulata (Ait.) Willd.", A. inokumai Murai & Kusaka'

C. intermedius (Gasparrini, 1851); C. americanus L. (Beal, 1890); C. glaber Spach (Sarauw, 1893); C. azureus Desf., C. delilianus Spach, C. fendleri A. Gray. C. microphyllus Michx., C. ovatus Desf. (Arzberger, 1910); C. welutinzcs Dougl. (Kellerman, 1911); C. foliosus Parry, C. rigidus Nutt., C. thyrsiflorus Esch. (Jepson, 1936); C. corddatus Kell., C. diverstifolius Kell., C. freshensis Dudley, C. impressus Trel., C. integerrimus Hook. & Am., C. parvifolius Trel., C. prostratus Benth. (Quick, 1944); C. crassifolius Torr., C. greggii A. Gray var. vestitus Greene, C. oliganthus Nutt. (Hellmers et al., 1955); C. leucodemis Greene (Hellmers & Kelleher, 1959); C. sanguineus Pursh (Furman, 1959); C. cuneatus (Hook.) Nutt., C. divaricatus Nutt., C. gloriosus Howell var. exaltatus Howell, C. griseus (Trel.) McMinn, C. incanus Torr. & Gray, C. j@sonii Greene, C. sorediatus Hook. & Am. (Delwiche et al., 1965)

H. rhamnoides L. (Oersted, 1865)

CEANOTHUS

HIPPOPHA&

ELAEAGNUS E. pungens Thunb. (Brunchorst, 1886-88); E. angustifolia L. (Nobbe et al., 1892); E. argentea Pursh (Kellerman, 1911); E. edulis Siebold ex E. May, E. rhamnoides (L.) A. Nelson (Spratt, 1912); E. longipes A. Gray (Milovidov, 1928); E. multiflora Thunb. (Fred et al., 1932); E. multi$ora Thunb. var. edulis (Carr.) Schneider, E. umbellata Thunb. (Roberg, 1933-4); E. macrophylla Thunb. (Hawker & Fraymouth, 1951); E. commutata Bernh. (Allen et al., 1964); E. pungms Thunb. var. simonii (Carr.) Nicholson (Allen & Allen, 1965)

M. gale L. (Brunchorst, 1886-8); M. cerifera L., M. pensylwanica Loisel., M. sapida Wall. var. longi- folia (Teysm. & Binned.) (Chevalier, 1900-2); M. rubra Sieb. & Zucc. (Shibata, 1902); M. asplenifolia L. (Arzberger, 1910); M. caroZinensisMil1. (Youngken, 1915); M. adenophora Hance (Shibata & Tahara, 1917); M. pubescens Willd.", M. javanica Blume (Becking, 1966); M. pilulifera Rendlee, M. serrata Lam."

C. muricata, C. quadvivalvis Labill. (Janse, 1897); C. equisetifolia L. (Kamerling, 1915); C. glaucn Sieber (Shibata & Tahara, 1917); C. stricta Ait. (Narasimhan, 1918); C. cunninghamiana Miq. (McLuckie, 1923); C. montana Leschen. (Parker, 1932); C. fraseriana Miq., C. Zepidophloia F. Muell. C, sumatrana Jungh., C. tenuissima Sieber ex. Spreng., C. triangularis (Mowry, 1933); C. huegeliana Miq. (Uemura, 1964); C. nodiflova Forst. f. (Allen & Allen, 1965); C. torulosa L.'

MYRICA

CASUARINA

SHEPHERDIA S. canadensis Nutt. (Nobbe & Hiltner, 1904); S. arzentea (Pursh) Nutt. (Warren, 1910)

C. intmmedia Matsum., C. japonica A. Gray (Shibata & Tahara, 1917); C. arborea Lindsay (Harris & Morrison, 1958); C. myvtifolia L. (Bond & Montserrat, 1958); C.plumosa W. R. B. Oliv., C.pte*idoides W . R. B. Oliv. (Morrison & Harris, 1959); C. angustissima Hook. f., C. kingiana Col., C. Zurida T. Kirk, C. pottsiana W. R. B. O h . , C. sarmentosa Forst. f. (Burke, 1963); C. thymifolia Humb. & Bonpl. ex Willd.'

DRYAS D. dvummondii Richardson (Lawrence, 1953) ; D. drummondii Richardson var. eglandulosa Porsild, D. integrifolia Vahl., D. octopetala L. (Lawrence et al., 1967)

* See text.

CORIARIA

80

Table 2.-continued

C . RODRIGUEZ -B ARRUECO

DISCARIA D. toumatou Raoul (Morrison & Harris, 1958)

PURSHIA P. glandulosa Curran, P. tridentata (Pursh) DC. (Wagle & Vlamis, 1961)

CERCOCARPUS C. betuloides Nutt. (Vlamis et al., 1964)

ARCTOSXAPH YLOS A . uva-ursi (L.) Spreng. (Allen et al., 1964)

The new list is provided in Table 2, where the genera are arranged chronologically according to the year in which nodulation was first reported within them. Similarly, within each genus the species are listed in the order in which they were first reported to be nodule-bearing, The authors cited are responsible for the record of nodulation in the one or more species preceding the citation. The plant names are as given by the authors cited and authorities for the names, if omitted by these authors, have been added" where this is possible. The lack of an authority in Table 2 signifies that either the name cited is ambiguous or no authority could be traced. It is probable that some of the specific names listed are synonyms for others also included; thus according to the Index Kewensis (Hooker & Jackson, 1893) the plant which Gasparrini (see Table 2) called Ceanothus intermedius should have been referred to C. ovatus Desf. or to C. anzericanus L., depending on the sense in which he was using 'intermedius'.

The evidence on which the species marked with an asterisk in Table 2 are recorded as nodule-bearing-for the first time, so far as the author is aware-is provided chiefly by reports kindly sent by botanists abroad to Professor G. Bond and made available to the author. Alnus jowllensis Kunth, Coriaria thymifolia Humb. & Bonpl. ex Willd. and Myricapubescens Willd. were reportedin 1965-6 by Mr G. S. Smit, Food andAgriculture Organisation, to bear nodules in Colombia. Ahus serruluta Willd. was reported in 1966 by Professor W. S. Silver, University of Florida, to be nodulated in south-eastern U.S.A. Myricu serrata Lam. was reported in 1966 by Dr G. D. Scott, University College of Rhodesia, to be nodulated in Rhodesia, while a similar report was received in respect of Myrica pilulifera Rendle from Mr M. Dale, Rhodesian Ministry of Agri- culture. Plants of Alnus inokumui Murai & Kusaka and Casuarina torulosa L., raised in the greenhouse by Mrs A. H. Mackintosh and the author respectively, have been observed to form nodules after appropriate inoculation; the seed of the Alnus sp. had been kindly supplied by Dr S. Uemura.

In the following summarized statement of the position revealed by Table 2, the number of species recorded to bear nodules is given first, while in parenthesis is the total number of species in the genus according to Willis (1966).

Alnus 27 (35), Ceanothus 31 (55 ) , Hippophag 1 (3), Elaeugnus 10 (454, Myrica 12 (35), Casuarinu 15 (45), Shepherdia 2 (3), Coriaria 12 (15), Dryas 3 (4), Discaria 1 (lo), Purshia 2 (2), Cercocarpus 1 (20), Arctostaphylos 1 (70).

* By the Editor.

ROOT NODULES ON NON-LEGUMINOUS PLANTS 81

Of the larger genera, the proportion of species recorded as bearing nodules is thus highest in Alnus and Coriaria, followed by Ceanothus. Despite the time that has passed since nodules were first observed in Casuarina, Elaeagnus and Myrica, only a small proportion of species appears to have been examined for nodules. There is also an obvious need for the examination of further species of Discaria, Cercocarpus and Arctostaphylos. In all, out of 342 species only 118 have been recorded to be nodule- bearing, the remainder being apparently unexamined. In the above numerical treat- ment the effect of the probable presence of synonyms in Table 2 has been ignored.

DISCUSSION

These records of nodulation refer in most cases to plants of the species in question which were growing in a particular locality or area, and it cannot be assumed that nodu- lation will be present on the species in other regions. The regularity of nodulation is an aspect on which more information is badly needed; and while the evidence suggests that some species, such as Alnus glutinosa, are regularly nodulated, this regularity does not extend to others. Thus White (1967) investigated the occurrence of nodules on Ceanothus cuneatus (Hook.) Nutt. in Oregon and California; soil-type appeared to be an important factor and, while in some types the majority of plants were nodulated, in serpentine soils very few were. A strange situation appears to exist in Dryas octopetala L. (Lawrence et al., 1967), which bears nodules in Alaska and Canada but not, according to present information, in Iceland or Scotland. Also, Arctostaphylos uva-ursi (L.) Spreng. bears nodules in Alaska (Allen et al., 1964), but the author knows of no record of their occurrence in Europe.

In only a few of the species listed in Table 2 have nodulated plants been tested for nitrogen fixation, but for at least one species of each genus, excepting Arctostaphylos, there is evidence (reviewed by Bond, 1963, 1967) based on long-term culture of plants (Plate 1B) or of short-term tests with 15N that nitrogen fixation occurs, provided that the plant is associated with its normal endophyte. I t is reasonable to believe that the same is probably true for the remaining species.

Chodat (1904) reported briefly that he had observed nodules similar to those of Alnus in a species (which he did not name) of Rhamnus. This, if it could be verified, would not be wholly unexpected, since as noted already (Table 1) two other genera in the Rhamna- ceae are nodule-forming. However, well-grown specimens of Frangula alnus Mill. (Rhamnus frangula L.) growing near Flanders Moss, Stirlingshire, proved to be without nodules, while plants of R. alaternus L. raised from seed in soil known to be infected with the Ceanothus nodule organism have formed no nodules after one year’s growth in the greenhouse of this Department. It is, however, very probable that further nodule- bearing non-leguminous genera still await discovery.

A question which obviously arises is why this group of nodule-bearing plants should be taxonomically so heterogeneous. In an attempt to explain this, Bond (1967) con- jectured that the link between the genera may be that they are all survivors from some earlier period when conditions in some way favoured the establishment of nodule symbioses, and that the necessary conditions have not arisen again.

6

82 C . RODRIGUEZ-BARRUECO ACKNOWLEDGEMENTS

The author is grateful to the Fundaci6n Juln March and to the Spanish Ministry of Education and Science for the award of scholarships, to Professor P, W. Brian for extending the facilities of his Department, to Professor G. Bond for his advice, and to Mr A. A. Bullock and Mr B. W. Ribbons for helpful suggestions. This paper is a contribution to the work of the PP (Production Processes) Section of the International Biological Programme.

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of the Eastern United States. Am.J. Phurm. 87: 391-398.

EXPLANATION OF PLATE

PLATE 1 A. Part of the root system of a plant (grown by Mrs A. H. Mackintosh) of Ceunothus velutinus Douglas var. luevigatus Torr. & Gray, showing the developing nodule-clusters. Natural size. Photo. Mr T. N. Tait. B. Plants of Alnus jorullensis Kunth after 28 weeks’ growth in water culture without combined nitro- gen. On the left, nodulated plants, on the right, non-nodulated plants. x 0.2. Photo. Mr R. Cowper. Reproduced from Fig. 3, p. 107, in article by C. Rodriguez-Barrueco, Fixation of nitrogen in root nodules of Alnus jorullensis H. B. & K., Phyton, 23: 103-110 (1966).

Bat. J . Linn. Sac., 62, 1

C. RODRIGUEZ-BAHRUECO

Plate 1

(Facing p . 84)