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Stem Nodulation in Legumes

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Stem Nodulation in Legumes Stem Nodulation in Legumes: Diversity, Mechanisms, and Unusual Characteristics Catherine Boivin, lbrahima Ndoye,2 Flore Molouba,I Philippe de Lajudie,I Nicolas Dupuy,l and Bernard Dreyfus1>* 'Laboratoire de Microbiologie, ORSTOM, B.P. 1386,.Dakar, Sénégal; *Université Cheikh Anta Diop, Département de Biologie Vegetale, Dakar, Senegal Referee: Dr. Frans J. de Bruijn, MSW-DOE Plant Research Laaboratory Michigan State University - To whom corespondence should be addressed. * ... ABSTRACT: Rhizobia can establish a nitrogen-fixing symbiosis with plants of the Leguminosae family. They elicit on their host plant the formation of new organs, called nodules, which develop on the roots. A few aquatic legumes, however, can form nodules on their stem at dormant root primordia. The stem-nodulating legumes described so far are all members of the genera Aeschynomene, Sesbania, Neptunia, and Discolobium. Their rhizobia1 symbionts be- long to four genera already described: Rhizobium, Bradyrhizobium, Sinorhizobium, and Azorhizobium. This review summarizes our current knowledge on most aspects of stem nodulation in legumes, the infection process and nodule development, the characterization and unusual features of the associated bacteria, and the molecular genetics of nodulation. Potential use as green manure in lowland rice of these stem-nodulating legumes, giving them agronomical importance, is also discussed. I KEY WORDS: stem-nbdulated legumes, Seibania, 'Aeschynomene,Azorhizob&&photosyn- .- .i:' ' thetic Bradyrhizobium, nitrogen fixation. ". I. INTRODUCTION % The symbiosis between leguminous h plants and soil bacteria of the Rhizobiaceae covery of profuse stem nodulation the fast- ' leads to the formation of nitrogen-fixing growing sahelian.,y m'ual " Tegume Sesbania nodules, generally exclusively appearing on rostrata. Since then, spontañeous aerial nodu- the roots. A few legume species, however, 'lation has been reported in four other also S. form nodules not only on their roots, but also species of Sesbynia, including punctata, at stem-located root primordia. The first native in Madagascar and closely related to , example of this phenomenon was first re- S. rostrata, and in 15 new species of ' ported in 1928 in Aeschynomene aspera L. Aeschynomene (Tablk 1). More recently, N2- by Hagerup,82and subsequently in 1936 in furing nydules have also been found on the 1 A. paniculata by von Suessenguth and items of the Brazilian legume DiscoZobium Beyer1e.P In addition, stem nodulation has puZcheZZ~m.~~~All known stem-nodulated been reported in Neptrtnia ~Zeracea'~~and legumes belong to only four genera: later in five other Aesclzyomene species (for Aeschynomene (22 species), DiscoZobium (1 references, see Table 1). species), Neptunia (1 species), and Sesbania 0735-2689/97/$.50 O 1997 by CRC Press LLC 1 r L -.-\. Fonds DoLumentaire ORSTOM -, - TABLE1 / Geographical Distribution and Grouping of Stem-Nodulating Legumes Legume Geographic distribution Plant groupa Ref. Aeschynomene Afraspera Africa I 2 Nilotica Africa I 2 Aspera Africa, S. Asia II 82 Ciliata Africa, S. America II 2 Cristata Africa, Madagascar II 98 Denticulata S. America II 53 Evenia S, America II 12 Indica Pantropical II 11, 175 Paniculata S. America II 168 Pratensis S. America II 53 Rudis S. America II 53 Scabra S. America II 53 Schimperi Africa II 2 Sensitiva Pantropical II 2, 53 Tambacoundensis Africa II 2 Uniflora Africa II 98 Villosa S. Amefica II 12 S. Fluminensis N. America II 106 . Virginica America II 55 Crassicaulis Africa III 2 Elaphroxylon Africa III 87 , . Pfundii Africa IlI 2 .. ..i., '.. Sesbania _.. Rostrata. Africa . I 48 .. 'y Punctata Madagascar I 48a Asia, Africa . 98 II . 2,:. 1 :- Africa .. .III ."48a .. ..~ . " i ' -JavaniCa.?Nept"-"ia S.E. Asia III 98 t. ,. .. ..k;:;;7:: I .. .. '_ 1. :ri.,L$!eacera Pantropbal 111 136 .. .. .. I. I$ m .' t:\ , 1:. -.! ,~. ' . ..:! : ., .'S. ' , o5 -.. , ~'...p,....:v . ..America .... .. III 1 . ,I ... ..a Legumes are grouped according to their ability to nodulate on the stem. I, nodulation all along the stem; II, nodulation mostly on the submerged part of the . stem but aerial nodulation possible; III, nodulation restricted to the lower and . .. submerged part of the stem. .. .. (5 species) (Table 1). These generally be- share the ability to grow in waterlogged soils, long to the subfamilies Papilionoideae swamps, or riverbanks of tropical regions of (Aesclzynomene,Discolobium, and Fesbania) Africa, South or Central America, and Asia, and Mimosoideae (Neptunia).*Aesclzynomene with the exception of A. ~ii-ginica,~~which i and Discolobium belong to the same tribe, grows in North America. The adaptation of the Aeschynomeneae. *O5 These legumes are these plants to flooded habitats has sparked mostly annual or perennial herbs or shrubs, a substantial interest in stem-nodulated and a few of them, such as A. elaplzroxylon legumes, particularly S. rostrata and p.' and D. prilchellum, are small trees. They afraspe~-al~*."~because these plants can be used __.I.. 'f? :"\ , . J -. , .. .... , . c t. -.. f. tropical regions of the world. The symbiosis are immersed in water.50J3 Depending on the between S. rostrata and its microsymbiont, host plant, the primordia can be distributed Azorhizobium caulinodans, has been dis- over the whole length of the stem or restricted cussed by de Br~ijn,~’and the potential ag- to its lower part. They remain either hidden ronomic applications of stem-nodulated le- under the stem cortex, often forming an epi- gumes used as green manure for rice has dermal dome, or they slightly pierce this struc- been reviewed recently by Ladha et aLg8 ture, showing a protruding dormant apex that During recent years, the characterization forms a circular cavity in the stem epidermis. of bacteria able to induce N,-fixing nodules Only protruding or scarcely piercing pri- on different genera and species of legumes mordia are accessible to rhizobial infec- has progressed considerably. Rhizobia1 tion, as bacteria enter the root primordium strains isolated from stem nodules have been by intercellular invasion (see Section V). shown to be quite diverse and to belong to Therefore, the nature and the localization four genera: Rtiizobiirnz, Bradyrlzizobiirnz, of the stem nodulation site are iìnportant Siiior~l~izobii~m,and A-orhizobi~m.~~,~~~~Oj.~~~factors for host sensitivity to rhizobial in- Moreover, rhizobial moleculär genetics and fection, and have been used for a distinc- molecular mechanisms leading to nodule tive classification of stem-nodulating le- formation have been investigated in consid- gume~.~,~~+~~Three groups of plants can be erable detail (see Reference 41). The distinguished (Table 1). Sesbania rostrata-A, caulinodans symbiosis Group I comprises aquatic legumes that has indeed become one of the most studied readily nodulate all along the stem. It in- models in plant-bacteria interactions. cludes S:.rostrata idS. punctata, with nodu- The aim of this article is to review the lation sites distributed in three or four verti-, current information on most aspects of stem cal rows all along the ~tem,4~~4~;~0,and nodulation, that is, the infection and nodula- Aeschynomene afraspera and A. <,nilotica, rion processes, the characterization and un- with th&primordiacove+g th6.whole...,.. .*.. stem. the- usual characteristics of bacteria respon- III this group, ‘the root .p&iioi.t+um...- .. I .. I .+ .? .c a~waysI ,.:.”,- jible for these processes, and the molecular protrudes throÜgh. .-c fhe ,qtex,;(epïde”qis), senetics of thë early’ steps óf&e plant-&- allowing e&y aerial bacterial-Lfection,. ...*.. i:’ * :robe interactions. I.. GrouplII, considered -as intermediate, comprises some Acschynomene species with primordia less developqd than those of group II. CLASSIFICATION OF STEM- 1. The root primordia, often located next‘to ~VODULATINGLEGUMES lenticels, scarcely penetrate the epidermis. Three typical species of this group are A. The most distinctive characteristic of stem- indica, A. sensitiva, and A. scabra.2 Their iodulating aquatic legumes is the presence of root primordia are still accessible to rhizobial predetermined nodulation sites on the stem.46 infection, and these spFcies nodulate mostly fie formation of these sites is totally inde- on the submerged part of the stem, but also lendent of rhizobial infection. Nodulation sites op the ae~alstem, though less readily than :orrespond to preformed dormant root pri- S. rostrata and A. afiaspera. Two species of nordia located on the stem.*58Anatomical Sesbania, S. speciosag8and S. pubescens,48a ;tudies have showed that these dm”t pri- could also belong to this group because nodu- nordia exhibit a typical root structure, a fact lation can be induced on aerial stem portions :onfirmed by the ability of these primordia to under high humidity conditions. 3 .._ I In group III, the root primordia remain belonging to groups 1and II (Sesbania and ' embedded in the stem cortical tissues as long Aeschynomene) would be the only species. as the dormancy of the root primordia is not unequivocally classified as true stem-nodu, broken by waterlogging. Nodules are never Iating legumes. The aquatic legumes of group found on aerial stems. Two typical species of III (Aeschynomene, Discolobium, and this group are A. elaphroxylon and A. crassi- Neptunia) could be an intermediate evolu- caulis, where stem nodulation is strictly re- tionary stage between true stem-nodulating stricted to the lower and submerged part of legumes and other plants that induce typical the stem. Discolobium pulchellum
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