Plant Physiol. 2007 Sprent 575 81

8/3/2019 Plant Physiol. 2007 Sprent 575 81

http://slidepdf.com/reader/full/plant-physiol-2007-sprent-575-81 1/7

Update on Legume Evolution

Legume Evolution: Where Do Nodules and MycorrhizasFit In? 1

Janet I. Sprent* and Euan K. JamesDivision of Applied and Environmental Biology, College of Life Sciences, University of Dundee,Dundee DD1 5EH, Scotland, United Kingdom

Recent ndings on legume biogeography and thetiming of evolution of key legume tribes have sup-ported a newview of the evolution of nodule processes.It is suggested that an initial infection process notinvolving root hairs led to two branches of legumenodule development, one that subsequently devel-oped transcellular infection threads (ITs) to carry bac-teria to young nodule cells and one in which such ITs

were not formed. Two types of nodules, with indeter-minate or determinate growth, evolved from each of these. Knowledge of the diversity of bacteria known tonodulate legumes and their relations with other bac-teria is expanding rapidly, posing new questions aboutnodulation in the eld. Ectomycorrhizas (ECMs) arefound in both nodulating and non-nodulating le-gumes and may be important in some environments.

This Update will address the following topics: (1)when andwherenodulation evolvedin legumes; (2)thekey processes that led to nodule structures found inextant legumes; (3) the growing number of nitrogen-xing bacteria known to nodulate legumes; and (4) the

role of ECMs and endomycorrhizas in certain legumegroups.

WHEN DID NODULATION EVOLVE?

Among the three subfamilies of legumes, nodulationhas long been known to be rare in Caesalpinioideae,common in Mimosoideae, and very common in Papil-ionoideae, a sequence thought to be consistent with theorder in which these subfamilies evolved (Allen andAllen, 1981). However, using a range of molecular datarooted using well-characterized legume fossils, Lavinet al. (2005) developed a chronology for legume evolu-tion in which they dated the origin of legumes at about59 million years before present, with all three subfam-ilies recognizable soon after. Particularly signicant fornodule evolution is that two major papilionoid groups,

the dalbergioid and genistoid legumes, appeared early,about 55 million years ago. The dalbergioid legumesare a monophyletic clade, one of whose distinguishingcharacteristics is the possession of aeschynomenoidnodules (Lavin et al., 2001; Fig. 1B). Aeschynomenoidnodules have no uninfected cells in the infected regionand their infection processes do not involve trans-cellular ITs. Although there is less information about

the genistoid legumes, many also appear to have thesecharacteristics, but with nodules having indeterminaterather than determinate growth (Fig. 1D). Other nodu-lated legumes, all of whose origins also date back to 55to 50 million years ago, appear to have transcellular ITsin their developing nodules, although these are notnecessarily involved in the infection process. Thus, twolines of nodule development appear to have beenestablished at about the same time.

Doyle and Luckow (2003) suggested that there mayhave been four separate events leading to nodulation inlegumes, but also pointed out that resolution of the basal, non-nodulating clades of legumes is still incom-

plete and may change in the coming years. So far thereis no additional information to resolve this question, soin this Update we concentrate on the processes leadingto formation of nodules, rather than the number of nodulation events.

WHERE DID NODULATION EVOLVE?

Schrireet al. (2005)analyzed thebiomeswhere extantlegumes arefound, andsuggested that therst legumesevolved in a semiarid area just north of the Tethys sea-way that separated the two major land masses existingat that time. Their evidence further pointed out some

anomalies that do not support the very appealinghypothesis that legumes may have moved betweenAfrica and South America via a northerly land bridge(gure 2 in Doyle and Luckow, 2003) Instead, it is nowthought that legumes could also have moved over largedistances of water, possibly by island hopping (fordiscussion, see Pennington et al., 2006) or by othermeans (such as in extreme weather events; Nathan,2006). This could explain, for instance, how a possiblesingle event leading to loss of nodulation in somespecies of Acacia, subgenus Aculeiferum, could result insome closely related non-nodulating species beingfound in North and South America and in parts of Africa (for discussion, see Sprent, 2007).

1 This work was supported in part by the Natural EnvironmentResearch Council (United Kingdom).

* Corresponding author; e-mail [email protected]; fax 44–1382–542989.

The author responsible for distribution of materials integral to thendings presented in this article in accordance with the policydescribed in the Instructions for Authors (www.plantphysiol.org) is: Janet I. Sprent ([email protected]).

www.plantphysiol.org/cgi/doi/10.1104/pp.107.096156

Plant Physiology, June 2007, Vol. 144, pp. 575–581, www.plantphysiol.org Ó 2007 American Society of Plant Biologists 575



In addition to asking when and where legumesevolved, it is also relevant to ask why nodulationevolved in some groups. As the process of nitrogen x-ation uses a signicant amount of the total carbon xed by the host plant, one driving force could have been anexcess of carbon dioxide coupled with a decit of com-

bined nitrogen. Several lines of evidence suggest that,at about 55 million years ago, when nodulate legumesmayhaveevolved,therewasamajorpeakinatmosphericcarbondioxide, temperature,andhumidity(Bowen etal.,2004; Sprent, 2007).

WHAT WERE THE KEY PROCESSES THAT LEDTO NODULE STRUCTURES FOUND INEXTANT LEGUMES?

First, compatible rhizobia needed to gain entry intothe legume root. The most widely studied mode of entry is via root hairs and involves transcellular ITs.

However, even the species that normally use this path-way may, under certain circumstances (usually a formof stress), become infected through breaks in the epi-dermis or wounds where lateral roots emerge (crackentry). Examples include white clover ( Trifolium repens;Mathesius et al., 2000), Lotus uliginosus (James and

Sprent, 1999), and the mimosoid aquatic legume Nep-tunia natans (5 Neptunia oleracea; Subba-Rao et al.,1995). For the latter species, the passage of bacteria between host cells and then the formation of trans-cellular ITs is clearly illustrated. We postulate that thedefault position for infection is directly between epi-dermal or cortical cells, and that this may lead to one of two patterns of nodule development. The rst neverinvolves transcellular ITs, although as bacteria pass between cells they may be surrounded by some of theextracellular components normally found in transcel-lular ITs (Brewin, 2004). Thismode of infection is foundin the dalbergioid and genistoid legumes, and mayaccount for approximately 25% of all legume genera

Figure 1. Structure of the main types of legumenodules. A, Sesbania macrantha root nodule.Although morphologically similar to the aeschy-nomenoid type of nodule seen in B, the infectedtissue contains uninfected cells and bacteria aretransmitted to infected cells by ITs. B, Aeschyno- mene rostrata stem nodule. This is typical of a

clade of dalbergioid legumes. ITs are neverformed and infected tissue contains no uninfectedcells. Infection occurs through breaks where lat-eral or adventitious root initials protrude and afew infected cells divide repeatedly. C, Mimosahimalayana . This structure is typical of all mimo-soid and many papilionoid nodules and in mostcases follows from root hair infection. There is aclear apical meristem (arrow), and the infectedtissue contains a mixture of infected and unin-fected cells. ITs convey bacteria to cells newlyformed by the meristem. D, Cytisus garden hy-brid, typical of many genistoid legumes. ITs arenever seen and infected tissue contains no unin-fected cells. There is a distinct apical meristem(arrow), which may divide, forming branchednodules or in some cases encircle the root ( Lupi- nus , Lotononis ). E, L. uliginosus , a typical deter-minate nodule as found in many members of tribeLoteae and in phaseoloid legumes such as soy-bean (Glycine max ). Meristematic activity is shortlived, infection is via root hairs, and infectedtissue contains uninfected cells. F, Erythrophleum ivorense , a typical caesalpinioid nodule with ablunt apex, a clear apical meristem (arrow), anduninfected cells in the infected tissue. Infectedcells retain bacteria in modied ITs, known asxation threads. They may branch repeatedly andbe lignied in the outer layers.

Sprent and James

576 Plant Physiol. Vol. 144, 2007



(Sprent, 2007). Considering that these groups includeimportant grain (some species of Lupinus, Arachis) andforage ( Stylosanthes) legumes, they have been sur-prisingly little studied. Arachis and Stylosanthes haveaeschynomenoid nodules, formed following crack in-fection where lateral (occasionally adventitious) roots

emerge. A few cells are infected by bacteria as they pass between cells.These host cells divide repeatedlyto givethe characteristic uniformly infected central tissue,with loss of meristematic activity (Fig. 1B; see Lavinet al. [2001] and Sprent [2001] for further details andreferences). Although the general structure of the in-determinate nodules of several genistoid legumes has been known for many years (Sprent, 2007, and refs.therein), their detailed development has only recently been described. Studies on Lupinus albus and Chamae-cytisus proliferus (now included in Cytisus) describeinfection directly via the epidermis or at the bases of roothairs(Vega-Herna ´ndez et al., 2001; Gonza ´lez-Samaet al., 2004), with a few host cells being infected andthese dividing repeatedly to give uniform infectedtissue, but with some cells retaining meristematic ac-tivity. Genista tinctoria nodules are very similar instructure to those of Cytisus (Fig. 1D), and Kalita et al.(2006) show clearly how infected cells in the apicalmeristem divide, formingnew nitrogen-xing tissueasthe nodule grows.

The second type of nodule development involvesdevelopment of transcellular ITs. Although generallyassociated with root hair infection, they may notalways be. Lonchocarpus muehlbergianus is a memberof the important tropical tribe Millettieae. It does notproduce root hairs and infection probably occurs be-

tween epidermal cells, with later formation of trans-cellular ITs (Cordeiro et al., 1996). Subsequently, as inindeterminate nodules with root hair infection, indi-vidual cells are infected by branches of the trans-cellular ITs and active nitrogen-xing tissue contains amixture of infected and uninfected cells. This patternof development has been studied in detail for manypapilionoid legumes and also appears common in atleast some Mimosoideae and all Caesalpinioideae (Fig.1, C and F). The position is similar in the determinatenodules of phaseoloid legumes (including Glycine, Pha-seolus, and Vigna) and Lotus in tribe Loteae, except thatmeristematic activity is short lived (Fig. 1E).

Entry of transcellular ITs into newly formed meri-stematic cells is accompanied by cessation of laterphases of mitotic division, so that cells become poly-ploid andgreatly enlarged, enabling them to house vastnumbers of nitrogen-xing bacteria. In indeterminatenodules, bacteria also show high levels of DNA repli-cation and this is accompanied by loss of viability. Indeterminate nodules this does not occur (Mergaertet al., 2006). However, endoreduplication also occurs inLupinus nodules, which do not have transcellular ITs(Gonza les-Sama et al., 2006).

The universal presence of uninfected cells in theinfected tissue of nodules withtranscellular ITs suggeststhat these may have a role in nodule functioning. This is

certainly true of determinate ureide-exporting nodules(those in the phaseoloid group) where these interstitialcellsare the mainsite ofsynthesis of the ureidesallantoinand allantoic acid, the chief export products from suchnodules(Sprent, 2001).Thefunctionof interstitial cells indeterminate Lotus nodules (these export amides, not

ureides) and indeterminate nodules is notclear, but theyseem to be a required structural feature. Further, geneticinformation for differentiation of nodules in the absenceof rhizobia, including the formation of large (normallyinfected) and small (normally interstitial) cells in thecentral tissue, is located in the host legume for at leastsome of the more recently evolved vicioid (galegoid)legumes (Pa et al. [1991] for alfalfa [ Medicago sativa];Blauenfeldt et al. [1994] for white clover; Gleason et al.[2006] for Medicago truncatula ; and Tiricine et al. [2006]for Lotus japonicus).

There have been occasional reports (Allen and Allen,1981; Bryan et al., 1995) that roots of the caesalpinioidlegumes Gleditsia and Peltophorum can be invaded byrhizobia, followed by formation of ITs but without theformation of nodules. Bryan et al. (1995) thought thatsuch processes could be an early stage in noduleevolutionandITsare certainlya feature of allnodulatedcaesalpinioidlegumes (Sprent, 2001). In nearlyallof thelatter, bacteria are not released from ITs and nitrogenxation takes place within modied ITs, called xationthreads (Sprent, 2001). This led to the suggestion(Sprent, 2007) that ITs were initially a defense responseto an invading organism. In the caesalpinioid genusChamaecrista, there is a spectrum of structures from x-ation threads in arboreal species to full release of bac-teria into symbiosomes in herbaceous species (Naisbitt

et al., 1992). A more detailed analysis of these speciesmight provide information on the evolution of symbio-somes. In evolutionary terms, the formation of trans-cellular ITs is a necessary prerequisite for root hairinfection. The role of cell wall materials in this processhas been reviewed by Brewin (2004).

Discussion on evolution of nodulation has hithertotaken into account presence or absence of nodules andnodule morphology (for example, Doyle and Luckow,2003). Determinate and indeterminate nodule growthhas proven to be a useful criterion. However, withinthese two groups, it is now clear that there are distinctdifferences in howindividual host cells areinfectedand

whether the infected cells are interspersed with unin-fected cells. Figure 2 summarizes a hypothesis thatlegume nodules were rst initiated from direct epider-mal or crack infection and that this led to two distinct branches of nodule development, one involving trans-cellular ITs and one not. Further details can be found inSprent (2007), available (free) online.

Although most legume databases are conned tospecieswitharoothairinfection,therearesomethataremore widely based. Of those tabulated by Stacey et al.(2006), one (PlantGDB; www.plantgdb.org) includesthe dalbergioid legume Arachis hypogea and the Aus-tralian legumeDB (Moolhuijzen et al., 2006) includesthe genistoid legume Lupinus angustifolius . As more

Legume Evolution: Where Do Nodules and Mycorrhizas Fit In?

Plant Physiol. Vol. 144, 2007 577



data are added to these databases, it may be possible todissect out the genes and processes responsible for themajor differences in nodule characteristics betweenthese and root hair-infected species and, hence, test ourhypothesis.

BACTERIA KNOWN TO NODULATE LEGUMES:ORDER INTO CHAOS?

Doyle and Luckow (2003) titled their paper ‘‘TheRest of the Iceberg,’’ indicating that the vast majorityof legumes were under (or often not) studied. Thesame could be said of the bacteria that nodulate

legumes, although this iceberg is melting rapidly. Inthe beginning (over a century ago), only one nodulat-ing bacterium had been described, Bacillus radicicola.Shortly after, fast- and slow-growing rhizobia weredistinguished and were subsequently given differentgeneric names ( Rhizobium and Bradyrhizobium). Thereare now several more genera of rhizobia, with numer-ous species, together with other bacteria from thea -proteobacteria, plus an increasing number from the

b -proteobacteria (Table I). Some of the latter ( Burkhol-deria phymatum STM815 and Burkholderia tuberumSTM678) can also x nitrogen in free-living culture(Elliott et al., 2007), and some Burkholderia spp. areknown to x nitrogen in association with grasses(Estrada de Los Santos et al., 2001). On the other hand,some ‘‘classic’’ rhizobia are now known to be able toinfect grasses, but with no good evidence that they xsignicant amounts of nitrogen in them (for review, seeGraham, 2007).

The close similarities between plant and animalinfection strategiesin a -proteobacteria, including prob-ably the best known example, Rhizobium and Brucella,

arediscussedbyBatut et al. (2004), with a moredetailedexamination of rhizobia and plant pathogens by Sotoet al. (2006). Horizontal (lateral) gene transfer in theform of genomic islands between various bacteria isconsidered byDobrindt etal. (2004). It is likelythat sucha transfer of symbiotic islands accounts for many of thenodulation reports in b -rhizobia. Bernier et al. (2003)suggested that the common opportunist human path-ogen Burkholderia cepacia, which can also enter wounds

Figure 2. A tentative scheme for theevolution of different types of nodulestructure. Dashed line, Pathway notfully demonstrated.

Table I. Nodulation of legumes by dened species of b -rhizobia

Species Origin of Type Strain Hosts Characteristics Reference

Burkholderiamimosarum

PAS44. Mimosa pigranodules in Taiwan.

Mimosa spp. Highly competitive for nodulationof invasive Mimosa spp.

Chen et al. (2006)

B. nodosa Br3437. Mimosa scabrellanodules in Brazil.

Mimosa spp. Closely related to B. mimosarum ,but not yet found outside Brazil.

Chen et al. (2007)

B. phymatum STM815. Machaerium lunatum (Papilionoideae)nodules in French Guiana.

Mimosa spp. andother mimosoidlegumes.

Very broad host range in theMimosoideae, but does not appearto nodulate Machaerium spp. FixesN2 ex planta.

Moulin et al. (2001);Vandamme et al. (2002);Elliott et al. (2007)

B. tuberum STM678. Aspalathus carnosa (Papilionoideae)nodules in South Africa.

Cyclopia spp.(Papilionoideae)

Does not appear to nodulateAspalathus spp. Fixes N2 ex planta.

Moulin et al. (2001);Vandamme et al. (2002);G.N. Elliott (personalcommunication)

Cupriavidus taiwanensis

LMG19424. Mimosa pudicanodules in Taiwan.

Mimosa spp. Broad host range, but not as wide asB. phymatum .

Chen et al. (2001);Elliott et al. (2007)

Sprent and James




in plants, causing disease, could well be studied usingalfalfa as a model system. Since then a strain of thisorganism has been isolated from nodules of species of Dalbergia in Madagascar (Rasolomampianina et al.,2005). Thus, many of the differences among bacteriainvading eukaryotes are rapidly turning into similari-

ties. It is not appropriate to go into details of thesesystems here, except to emphasize that not only arethere numerous legume plants whose nodulation de-tails are largely unknown (Doyle and Luckow, 2003;Sprent, 2007), but also there are far more nodulating bacteria than have yetbeen studied for their interactionwith host genotypes. If the benets of nitrogen xationin legumes are to be more widely understood andexploited, especially in some tropical soils, these inter-actions need to be explored.

It is too earlyto speculate how these b -rhizobia relateto either legume phylogeny or evolution, but it may berelevant that, so far, they have only been found intropical areas.

MYCORRHIZAS AND LEGUMES

There are two main types of mycorrhiza in legumes,arbuscular mycorrhizas (AMs) and ECMs. As AMsevolved long before legumes, we may assume that alllegumes have the potential to produce them ( Lupinusis the only known legume genus in which this abilityhas been lost). Similarities between initial processesinvolving infection by AM fungi and rhizobia are beingextensively investigated and reviewed (Kinkema et al.,2006; Stacey et al., 2006), and will not be considered

here. Further, some of these processes, including endo-reduplication, may have been hijacked by root-knotnematodes (Weerasinghe et al., 2005). The occurrenceof ECMs in legumes is sporadic. The typical ECM,with a sheathing mantle and Hartig net, is character-istic of some of the Caesalpinioideae. In the analysis of Lavin et al. (2005), a branch of this subfamily that isnon-nodulating has one section that includes onlyECM genera, the others being AM (Sprent 2007). Thissuggests a common origin of ECMs in this branch, theplants of which are mainly trees of African rainforests.Here, their ECMs are found principally in the litterlayers, as are nodules on some of the few, but pro-

fusely, nodulated legume species (Sprent, 2005). ECMlegumes are a vital part of the phosphorus dynamics of such forests (Newbery et al., 1997). Although it used to be thought that ECMs and nodulation in legumes weremutually exclusive (Malloch et al., 1980), this is nowknown not to be true. For example, Ho ¨gberg and Pierce(1986) reported that Pericopsis angolensis(a woody speciesin papilionoid tribe Sophoreae), normally ECM and non-nodulating, can also form AMs on plants that can thenalso nodulate (as can other species of this genus; Sprent,2001). Even ECM legumes that cannot nodulate may beable to form AMs in certain locations (Moyersoen andFitter, 1999), a feature that may enable them to exchangenutrients with nodulated AM legumes in some tropical

forests (Sprent, 2005, 2007). A switch between forms of mycorrhiza according to environment is known fromother, nonlegume species, such as Populus angustifolia(Gehring et al., 2006). The genome of another species of this genus, Populus trichocarpa, has recently been pub-lished (Tuskan et al., 2006), raising the possibility that

genes controlling different types of mycorrhizal forma-tion may soon be identied. Before these can be alignedwith legumes, however, we need information on thegenomes of legume species that can form both types.

There are reports of ECMs in the other legumesubfamilies, in plants from soils rather low in nutrientsandwater andwithout a pronounced litter layer. AllareAustralian endemics, although some acacias can formECMs with local fungi when grown in countries as farapart as Brazil and East Africa (Sprent, 2001, and refs.therein). Papilionoid tribes Mirbelieae and Bossiaeeaehave a number of genera capable of forming typicalECMs and rather looser associations, as found inspecies of Australian Acacia, subgenus Phyllodineae(Alexander, 1989; Sprent, 2001). All can also formAMs and, in some cases, cluster roots. Thus, manylegumes appear to have the potential to form bothAMs and ECMs, as do many other nodulated membersof the Rosid 1 clade (Wang and Qui [2006] list these,although not using the cladistic analysis of Soltis et al.[2000]).

Thus, evidence now suggests that legumes are veryversatile in their symbioses. Unfortunately, the molec-ular aspects of ECM development have been far lessstudied than those for AMs, with no studies at all onECMs in legumes. Nodulation hasa signicant require-ment for phosphorus (P), so it would seem sensible to

have P-acquiring symbioses (AM and/or ECM) near tonodules. This is true of AMs, and there have been occa-sional reports that AM hyphae colonize nodules. How-ever, this appears only to be true for nonfunctionalnodules (Scheublin and van der Heijden, 2006; ourgroup has sectioned many thousands of nodules fromhundreds of legume genera, and we have never seenAM hyphae in them). On the other hand, ECMs may bespatially separated from nodules (for example, in thecase of P. angolensis [above]). Cluster roots can assist inthe uptake of P, and, in soils with low available P, nod-ules are formed among them (Schulze et al. [2006] forL. albus; F. Dakora [personal communication] for Aspa-

lathus linearis ).Received January 19, 2007; accepted March 5, 2007; published June 6, 2007.

LITERATURE CITED

Alexander IJ (1989) Systematicsand ecology of ectomycorrhizal legumes. InCH Stirton, JL Zarucchi, eds, Advances in Legume Biology. Monographsin Systematic Botany, Vol 29. Missouri Botanical Garden, St. Louis,pp 617–624

Allen ON, Allen EK (1981) The Leguminosae: A Source Book of Charac-teristics, Uses and Nodulation. University of Wisconsin Press, Madison,WI/Macmillan Publishing, London

Batut J, Andersson GE, O’Callaghan DO (2004) The evolution of chronicinfection strategies in the a -proteobacteria. Nat Rev Microbiol 2:933–945





Bernier SP, Silo-Suh L, Woods DE, Ohman DE, Sokol PA (2003) Compar-ative analysis of plant and animal models for characterization of Burk-holderia cepaciavirulence. Infect Immun 71: 5306–5313

BlauenfeldtJ, Pa J, Gresshoff PM, Caetano-AnollesG (1994)Nodulation of white clover ( Trifolium repens) in the absence of Rhizobium. Protoplasma179: 106–110

Bowen GJ, Beerling DJ, Koch PL, Zachos JC, Quattlebaum T (2004) Ahumid climate state during the Palaeocene/Eocene thermal maximum.

Nature 432: 495–499Brewin NJ (2004) Plant cell wall remodelling in the Rhizobium-legume

symbiosis. CRC Crit Rev Plant Sci 23: 293–326Bryan JA, Berlyn GP, Gordon JC (1995) Towards a new concept of the

evolution of symbiotic nitrogen xation in the Leguminosae. Plant Soil186: 151–159

Chen W-M, de Faria SM, James EK, Elliott GN, Lin K-Y, Sheu S-Y, Sprent JI,Vandamme P (2007) Burkholderia nodosasp. nov., isolated from root nodulesofthe woody Brazilianlegumes Mimosabimucronataand Mimosascabrella.IntJSyst Evol Microbiol (in press)

Chen W-M, James EK, Coenye T, Chou J-H, Barrios E, de Faria SM, ElliottGN, Sheu SY, Sprent JI, Vandamme P (2006) Burkholderia mimosarumsp.nov., isolated from root nodules of Mimosa spp. from Taiwan and SouthAmerica. Int J Syst Evol Microbiol 56: 1847–1851

Chen W-M,LaevensS, LeeTM, Coenye T, de VosP,MergeayM, VandammeP(2001) Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa

species and sputum of a cystic brosis patient. Int J Syst Evol Microbiol 51:1729–1735Cordeiro L, Sprent JI, McInroy SG (1996) Some developmental and

structural aspects of nodules of Lonchcarpus meuhlbergianus. Naturalia(Sao Paulo) 21: 9–21

Dobrindt U, Hochhut B, Hentchel U, Hacker G (2004) Genomic islands inpathogenic and environmental microorganisms. Nat Rev Microbiol 2:414–424

Doyle JJ, Luckow M (2003) The rest of the iceberg: legume diversity in aphylogenetic context. Plant Physiol 131: 900–910

Elliott GN, Chen W-M, Chou J-H, Wang H-C, Sheu S-Y, Perin L, Reis VM,MoulinL, SimonMF,Bontemps C,et al (2007)Burkholderia phymatumis ahighly effective nitrogen-xing symbiont of Mimosa spp. and xesnitrogen ex planta. New Phytol 173: 168–180

Estrada de Los Santos P, Bustillos-Cristales R, Caballero-Mellado J (2001)Burkholderia, a genus rich in plant-associated nitrogen xers with wide

environmental and geographic distribution. Appl Environ Microbiol 67:2790–2798Gehring CA, Mueller RC, Whitham TG (2006) Environmental and genetic

effects on the formation of ectomycorrhizal and arbuscular mycorrhizalassociations in cottonwoods. Oecologia 149: 158–164

GleasonC, Chaudhuri S, YangT, Mun ˜ ozA, PoovaiahBW,Oldroyd GED (2006)Nodulation independent of rhizobia induced by a calcium-activated kinaselacking autoinhibition. Nature 441: 1149–1152

Gonza´ lez-Sama A, Coba de la Pen ˜ a T, Kevel Z, Mergaert P, Lucas M, deFelipe MR, Kondorosi E, Pueyo JJ (2006) Nuclear DNA endoredupli-cation and expression of the mitotic inhibitor Ccs52 associated todeterminate and lupinoid nodule organogenesis. Mol Plant MicrobeInteract 19: 173–180

Gonza´lez-Sama A, Lucas MM, de Felipe MR, Pueyo JJ (2004) An unusualinfection mechanism and nodule morphogenesis in lupin ( Lupinus albus L.).New Phytol 163: 371–380

Graham PH (2007) Ecology of the root nodule bacteria of legumes. In MJDilworth, EK James, JI Sprent, WE Newton, eds, Leguminous Nitrogen-Fixing Symbioses. Springer, Dordrecht, The Netherlands (in press)

Ho ¨ gberg P, Pierce GD (1986) Mycorrhizas in Zambian trees in relation to hosttaxonomy, vegetation type and successional patterns. J Ecol 74: 775–785

James EK, Sprent JI (1999) Development of N 2-xing nodules on the wetlandlegume Lotus uliginosus exposed to conditions of ooding. New Phytol 142:219–231

Kalita M, Ste ´pkowski T, q otocka B, Malek W (2006) Phylogeny of nodu-lation genes and symbiotic properties of Genista tinctoria bradyrhizobia.Arch Microbiol 186: 87–97

Kinkema M, Scott PT, Gresshoff PM (2006) Legume nodulation: success-ful symbiosis through short- and long-distance signalling. Funct PlantBiol 33: 1–15

Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary ratesanalysis of Leguminosae implicates a rapid diversication of lineagesduring the tertiary. Syst Biol 54: 574–594

Lavin M, Pennington RT, Klitgaard BB, Sprent JI, de Lima HC, Gasson PE(2001) The Dalbergioid legume (Fabaceae): delimitation of a pantropicalmonophyletic clade. Am J Bot 88: 503–533

Malloch DW, Pirozynski KA, Raven PH (1980) Ecological and evolution-ary signicance of mycorrhizal symbiosis in vascular plants (a review).Proc Natl Acad Sci USA 77: 2113–2118

Mathesius U, Weinman JJ, Rolfe B, Djordjevic MA (2000) Rhizobia caninduce nodules in white clover by ‘hijacking’ mature root cortical cells

activated during lateral root development. Mol Plant Microbe Interact13: 170–182

Mergaert P, Uchiumi T, Alunni B, Evanno G, Cheron A, Catrice O,Mausset A-E, Barloy-Hubler F, Galibert F, Kondorosi A, et al (2006)Eukaryotic control on bacterial cell cycle and differentiation in theRhizobium-legume symbiosis. Proc Natl Acad Sci USA 103: 5230–5235

Moolhuijzen P, Cakir M, Hunter A, Schibeci D, Macgregor A, Smith C,Francki M, Jones MGK, Appels R, Bellgard M (2006) LegumeDB bioinformatics resource: comparative genome analysis and novel cross-genera marker identication in lupin and pasture legume species.Genome 49: 689–699

Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the b -subclass of Proteobacteria. Nature 411:948–950

Moyersoen B, Fitter AH (1999) Presence of arbuscular mycorrhizas in typicallyectomycorrhizalhost speciesfrom Cameroonand NewZealand.Symbiosis 8:

247–253Naisbitt T, James EK, Sprent JI (1992) The evolutionary signicance of thegenus Chamaecrista as determined by nodule structure. New Phytol 122:487–492

Nathan R (2006) Long-distance dispersal of plants. Science 313: 786–788Newbery DMcC, Alexander IJ, Rother JA (1997) Phosphorus dynamics in

a lowland African rain forest: the inuence of ectomycorrhizal trees.Ecol Monogr 67: 367–409

Pa J, Caetano-Anolles G, Graham ET, Gresshoff PM (1991) Ontogeny andultrastructure of spontaneous nodules in alfalfa ( Medicago sativa).Protoplasma 162: 1–11

Pennington RT, Richardson JE, Lavin M (2006) Insights into the historicalconstruction of species-rich biomes from dated plant phylogenies,neutral ecological theory and phylogenetic community structure. NewPhytol 172: 605–616

Rasolomampianina R, Bailly X, Fetiarison R, Rabevohitra R, Be ´na G,

Ramaroson L, Raherimandimby M, Moulin L, de Lajudie P, Dreyfus B,et al (2005) Nitrogen-xing nodules from rose wood legume trees(Dalbergia spp.) endemic to Madagascar host seven different genera belonging to a - and b -Proteobacteria. Mol Ecol 14: 4135–4136

Scheublin TR, van der Heijden MGA (2006) Arbuscular mycorrhizal fungicolonise non-xing root nodules of several legume species. New Phytol172: 732–738

Schrire BD, Lavin M, Lewis GP (2005) Global distribution patterns of theLeguminosae: insights from recent phylogenies. Biol Skr 55: 375–422

Schulze J, Temple G, Temple SJ, Beschow H, Vance CP (2006) Nitrogenxation by white lupin under phosphorus deciency. Ann Bot (Lond)98: 731–740

Soltis DE, Soltis PS, Chase ME, Mort ME, Albach DC, Zanis M,Savolainen V, Hahn WH, Hoot SB, Fay MF, et al (2000) Angiospermphylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot J LinnSoc 133: 381–461

Soto MJ, Sanjua ´n J, Olivares J (2006) Rhizobia and plant-pathogenic bacteria: common infection weapons. An Microbiol (Rio J) 152:3167–3174

Sprent JI (2001) Nodulation in Legumes. Royal Botanic Gardens, Kew, UKSprent JI (2005) West African legumes: the role of nodulation and nitrogen

xation. New Phytol 167: 326–330Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic

perspective of the occurrence of nodulation. New Phytol 171: 11–25Stacey G, Libault M, Brechenmacher L, Wan J, May GD (2006) Genetics

and functional genomics of legume nodulation. Curr Opin Plant Biol 9:110–121

Subba-Rao NS, Mateos PF, Baker D, Pankratz HS, Palma J, DazzoFB, Sprent JI (1995) The unique root-nodule symbiosis between Rhizo-bium and the aquatic legume Neptunia natans (L.f.) Druce. Planta 196:311–320

Tiricine L, Imaizumi-Anraku H, Yoshida S, Murakami Y, Madsen LH,Miwa H, Nakagawa T, Sandal N, Albrektsen AS, Kawaguchi M, et al

Sprent and James




(2006) Deregulation of a Ca 21 /calmodulin-dependent kinase leads tospontaneous nodule development. Nature 441: 1153–1156

Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, HellstenU, Putnam N, Ralph S, Rombauts S, Salamov A, et al (2006)The genome of black cottonwood, Populus trichocarpa. Science 313:1596–1604

Vandamme P, Goris J, Chen WM, de Vos P, Willems A (2002) Burkholderiatuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots

of tropical legumes. Syst Appl Microbiol 25: 507–512

Vega-Herna ´ndez MC, Pe ´ rez-Galdona R, Dazzo FB, Jarabo-Lorenzo A,Alfayate MC, Leon-Barrios M (2001) Novel infection process in theindeterminate root nodule symbiosis between Chamaecytisus proliferus(tagasaste) and Bradyrhizobium sp. New Phytol 150: 707–721

Wang B, Qui YL (2006) Phylogenetic distribution and evolution of mycorrhizasin land plants. Mycorrhiza 16: 299–363

Weerasinghe RR, Bird DM, Allen NS (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus

japonicus. Proc Natl Acad Sci USA 102: 3147–3152



Plant Physiol. 2007 Sprent 575 81

Documents

Transcript of Plant Physiol. 2007 Sprent 575 81