Bot. J. Linn. SOC.,62, pp. 77-84. With Iplate
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
Records of nodulated species
Discussion
.
Acknowledgements
References
.
.
.
.
.
.
.
.
PAGE
*
.
77
78
81
82
82
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 1 A shows early stages in the formation of such noduleclusters 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 nonleguminous 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.
C . RODRIGUEZ-BARRUECO
78
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, collectivelythey form a very heterogeneous group.
Table 1. Non-leguminous genera with nodule-bearing species, and their classification
according to Engler (1964)
Genus
Family
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
Order
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 nonleguminous 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 publication 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,
ROOTNODULES
ON NON-LEGUMINOUS
PLANTS
79
Table 2. Non-leguminous Angiosperms reported to bear Alnus-type root nodules
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 (Castellanos, 1944); A. multinervis Matsum., A. sieboldiana Matsum., A. tinctoria Sarg. var. glabra Call.
(Uemura, 1 9 5 2 ~ ) ;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'
CEANOTHUS
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)
HIPPOPHA&
H. rhamnoides L. (Oersted, 1865)
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)
MYRICA
M. gale L. (Brunchorst, 1886-8); M . cerifera L., M. pensylwanica Loisel., M. sapida Wall. var. longifolia (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."
CASUARINA
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.'
SHEPHERDIA
S. canadensis Nutt. (Nobbe & Hiltner, 1904); S. arzentea (Pursh) Nutt. (Warren, 1910)
CORIARIA
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.
C. RODRIGUEZ
-BARRUECO
80
Table 2.-continued
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. Alnusjowllensis Kunth, Coriaria thymifolia Humb. & Bonpl. ex Willd. and
MyricapubescensWilld. 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 Agriculture. 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.
ROOTNODULES
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. I n all, out of 342 species only 118 have been recorded to be nodulebearing, the remainder being apparently unexamined. I n the above numerical treatment 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 nodulation 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 15Nthat 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 Rhamnaceae are nodule-forming. However, well-grown specimens of Frangula alnus Mill.
(Rhamnusfrangula 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 nodulebearing non-leguminous genera still await discovery.
A question which obviously arises is why this group of nodule-bearing plants should
be taxonomically so heterogeneous. I n an attempt to explain this, Bond (1967) conjectured 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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EXPLANATION OF PLATE
PLATE1
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 nitrogen. 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)