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2 Chpter 3 Tolernce to Drought in Leguminous Plnts Medited y Rhizoium nd Brdyrhizoium Alln Klynger d Silv Loto, Joquim Alenísio Gomes d Silveir, Roerto Cezr Loo d Cost nd Cândido Ferreir de Oliveir Neto Additionl informtion is ville t the end of the chpter 1. Introduction The wter vilility is considered the climtic fctor with lrge effect on griculturl productivity, eing responsile to determine species distriution in different climte zones round the gloe [1]. Effects of drought depend of plnt development stge, intensity, nd durtion of the wter restriction. In other hnd, plnt dptive strtegies will determine the tolernce level, nd consequently your survivl on these conditions of indequte wter supply [2]. Wter deficit is n iotic fctor tht ffects the griculturl production with high frequency nd intensity, influencing spects relted to plnt development, such s decrese in photosynthesis rte, reduction in lef re [3], nd stomt closing [4]. Crops normlly present performnce ffected y wter deficiency, which cn cuse lower growth nd development (Figure 1), with progressive reduction in lef dry mtter [5] nd consequent repercussion on production prmeters, such s numer of grins nd pods per plnt. Root system presents complex strtegy iming to mintin wter supply in conditions of wter deficit, y incresing the root elongtion rte nd completely inhiiting the shoot [6]. On the other hnd, plnts growing in low wter potentils normlly present root thinner [7], nd this morphologicl modifiction is n dpttion to increse wter sorption efficiency. Therefore, comintion of chnges in morphologicl, physiologicl nd iochemicl levels re necessry to plnt survivl in environments ffected y drought d Silv Loto et l.; licensee InTech. This is n open ccess rticle distriuted under the terms of the Cretive Commons Attriution License ( which permits unrestricted use, distriution, nd reproduction in ny medium, provided the originl work is properly cited.

3 50 Responses of Orgnisms to Wter Stress control drought Figure 1. Visul spect of shoot in Phseolus vulgris plnts exposed to drought y four dys. The iologicl fixtion of nitrogen is the cpcity of n orgnism to divide the molecule of nitrogen (N 2 ) nd to comine hydrogen toms (H + ), forming mmonium (NH 4+ ) [8], eing crried out y distinct group of microorgnisms, singly or under symiosis. The Brdyrhizoium nd Rhizoium genders re descried s soil cteri tht hve ility to infect root hir of leguminous plnts, nd it to induce nodule formtion (Figure 2), with susequent fixtion of nitrogen [9]. Figure 2. Visul spect of root system of Vign unguicult plnts inoculted with Brdyrhizoium. The red rrows indicte nodules formed fter infection process.

4 Tolernce to Drought in Leguminous Plnts Medited y Rhizoium nd Brdyrhizoium 51 The persistence of rhizoil strins, nd their symiotic performnce in current nd susequent sesons re ffected y numerous iotic nd iotic fctors [10], with drought stress nd nitrogen deprivtion, eing mong the most significnt in mny prts of the world [11]. Other importnt fctor is the root exudtion ility, which it will determine plnt microe ssocitions so tht the survivl nd tolernce of rhizoi during wter restriction. Molydenum is n essentil element for soil microorgnisms, since it serves s cofctor for different enzymes involved in the metolism of nitrogen, cron nd sulfur. Before the synthesis of molydoenzymes, uptke of molydte, which is the more stle form of molydenum), its ctivtion to n pproprite form, nd its incorportion into the orgnic frction of the molydenum-cofctors, re required [12]. The presence of molydenum is necessry during formtion of severl proteins, including the nitrogense, the molydoenzyme tht reduces tmospheric dinitrogen (N 2 ) into mmoni (NH 4+ ) [13]. This cterium is lso cple of denitrifiction, vi nitric oxide (NO) nd nitrous oxide (N 2 O) to N 2, when the cells re cultured under oxygen-limiting conditions [14]. The first rection of denitrifiction, is crried out y the periplsmic Mo-contining nitrte reductse [15]. In ddition, the rection under norml conditions is descried s N e + 8 H MgATP 2 NH 3 + H MgADP + 16Pi. The enzyme mechnism requires reduction of the Fe protein y electron donors such s ferredoxin nd flvodoxin, trnsfer of single electrons from the Fe protein to the MoFe protein (which is dependent on MgATP hydrolysis) nd, finlly, internl electron trnsfer in the MoFe protein y the P cluster to the FeMo cofctor sustrte-inding site. Ech electrontrnsfer step requires n oligtory cycle of ssocition of the Fe nd MoFe proteins to form complex (Figure 3), fter which the two components dissocite [16]. Figure 3. Schemtic representtion of the nitrogense Fe protein cycle. The Fe protein dimer is shown in light lue with the cue representing the [4Fe 4S] cluster coloured lck to indicte the reduced form nd red to represent the oxidized form. The α nd β suunits of the MoFe protein re depicted s ornge nd pink, respectively, the yellow squres represent the P cluster nd the lck dimond represents the FeMo cofctor. Chnges in the oxidtion stte of the MoFe protein re not shown [16].

5 52 Responses of Orgnisms to Wter Stress Severl leguminous such s Vign unguicult nd Cicer rietinum re considered tolernt to wter deficit, nd importnt mechnisms were developed y this species to tolerte indequte wter supply. For exmple, iochemicl modifictions in cron metolism, such s increse in sucrose [17], s well s significnt interference in nitrogen metolism, like reduction of solule proteins [5] nd increse in totl mino cids [18] contriute to osmotic djustment of these plnts (Figure 4). Figure 4. Glutmine synthetse ctivity (), totl solule mino cids () nd totl solule proteins (c) in Vign unguicult plnts cv. Vit 7 sujected to 4 dys of wter restriction nd 2 dys of rehydrtion. Mens followed y the sme letter re not significntly different y the Tukey test t 5% of proility. The rs represent the men stndrd error nd the rrow the rrow indictes the rehydrtion point [5].

6 Tolernce to Drought in Leguminous Plnts Medited y Rhizoium nd Brdyrhizoium Ojective Aims of this chpter is to define (i) wter deficiency nd iologicl fixtion of nitrogen, to explin (ii) s this symiotic process cn promote eneficil repercussions to plnt nd microorgnism, nd to present (iii) the ttenution of negtive impcts on nodule nd plnt, esides nitrogen compounds nd morphologicl prmeters of plnts exposed to wter restriction. 3. Wter mintennce in lef nd nodule produced y inocultion Drought is environmentl component tht ffect crop yields worldwide. In nture, this stress is multifceted prolems tht re usully ssocited with other dverse circumstnces, which limit plnt performnce such s wter shortge nd nutrient deficits. In order to ssess the osmotic stress, Sssi et l. [19] monitored two Phseolus vulgris cultivrs inoculted with Rhizoium, eing cvs. Flmingo (tolernt) nd Cv. Coco Blnc (sensitive). Lef osmotic potentil (Ψo) decresed in stressed plnts in oth cultivrs. A minimum vlue of 2.3 MP ws reched in Cv. Flmingo plnts under mnnitol-induced osmotic stress (Figure 5 A). Ψo decresed in stressed nodules, reching 1.3 MP in Cv. Coco Blnc nd 1.7 MP in Cv. Flmingo (Figure 5 B). Therefore, Cv. Flmingo showed etter osmotic djustment response to osmotic stress oth in leves nd nodules [19]. Figure 5. Vrition of osmotic potentil (Ψo) in response to osmotic stress in leves (A) nd nodules (B) medited y 50 mm mnnitol. Vlues represents men ± SE (n=6) [19]. In control leves of oth cultivrs, RWC remined close to 80% (Figure 6 A). After 15 dys of osmotic tretment, RWC ws 65%in mnnitol-treted plnts of Cv. Flmingo, nd only

7 54 Responses of Orgnisms to Wter Stress 45% in Cv. Coco Blnc. These results indicte tht osmotic stress cused n importnt reduction in shoot wter supply. The sme trend ws oserved in nodules (Figure 6 B). Indeed, dt showed decresed nodule RWC in oth stressed cultivrs. This decrese ws higher in Cv. Coco Blnc treted nodules [19]. Figure 6. Effect of mnnitol-induced osmotic stress on reltive wter content (RWC) in Flmingo nd Coco lnc en cultivr leves (A) nd nodules (B). Vlues represents men ± SE (n=6) [19]. Mnnitol-induced wter deficit produced sustntil dehydrtion tht led to decresing Ψo (Figure 6). The decrese in Ψo is considered potentil mechnism of cellulr drought resistnce s it enles turgor mintennce nd growth continution [20]. Cv. Flmingo exhiited lower Ψo under osmotic tretment. It ws le to uptke more wter nd then grow more when exposed to decresed Ψo, thus it turned out to e etter drought tolernt cultivr thn Cv. Coco Blnc [21]. This my e ttriuted to mintennce of the lef nd nodule wter sttus under stressed conditions (Figure 5). Severl mechnisms could e involved in contriuting to wter retention. 4. Brdyrhizoium meliortes negtive effects in plnts exposed to drought The reltionship etween the wter sttus in the plnt nd N2 fixtion, minly under wter stress, nd the chnges in nodule morphology hve een studied in some temperte legumes [22]. However, tropicl legumes growing in rid regions, hve not received dequte ttention. Even where informtion is ville, the degree of wter stress in the plnts ws not clerly defined, which mkes it difficult to mke comprisons. The structurl sis for the differ

8 Tolernce to Drought in Leguminous Plnts Medited y Rhizoium nd Brdyrhizoium 55 ence in sensivity of N2 fixtion in tropicl legumes, under wter stress, is not clerly understood [23]. Bsed in these prolems reported, Figueiredo et l. [24] investigted Vign unguicult plnts exposed to 3 inocultion forms (BR-2001, EI-6, nd control) comined with 6 different degrees of wter stress (-1.5, -2.0, -4.0, -6.0, -8.0, nd kp). Wter deficit response in cowpe ppers to e directly relted to reduction in nodule mss (Tle 1), which my (fter severe stress, S6) hve ffected nodule structurl constituents. However, in moderte stress (S3) the impct on nodule wter content ws higher thn on the chnges in nodule mss [24]. (1) For S1 to S6 see Tle 1. *, **Significnt t the 0.05 nd 0.01 proility level. In ech column (lower letters) nd in ech line (cpitl letters), the mens followed y the sme letter do not differ sttisticlly (p< 0.05) from ech other, ccording to Tukey s test Tle 1. Nodule dry mtter (NDM) nd nodule wter content (NWC) in cowpe with (BR-2001 nd EI-6) nd without (C) Brdyrhizoium spp. inocultion t different degrees of wter stress [24]. 5. Interference positive on nitrogen compounds of plnts inoculted nd exposed to wter deficit Cowpe (Vign unguicult [L.] Wlp.) is leguminous with high protein content, lrge cpcity of fixtion of the tmospheric nitrogen (N 2 ) nd low requirements to soil fertility [25], eing frequently cultivted y frmers in Northern nd Northestern regions of the Brzil. This species constitutes the min susistence culture, eing the grin used s protein source in feeding [26]. Cowpe presents importnt gronomicl chrcteristics, such s rusticity nd precocity, esides eing considered plnt dpted to conditions of limited or insufficient wter vilility [27].

9 56 Responses of Orgnisms to Wter Stress Beneficil effects proportioned y the inocultion on growth prmeters s lef, stem nd root re lrgely explored nd well known in leguminous plnts [28-30], ut informtions more specific of this symiotic process on essentil compounds such s mino cids nd proteins re limited. Figueiredo et l. [24] report tht inocultion using Brdyrhizoium cn llevite the negtive consequences in Vign unguicult plnts induced to wter deficiency, ut study conducted y Serrj nd Sinclir [31] reveled tht wter supply presents repercussion on symiotic efficiency. Bsed on this overview, Bros et l. [32] crried out study iming to investigte if nitrogen compounds exercise influence on ccumultion of dry mtter in Vign unguicult plnts exposed to comined ction of inocultion nd wter deficit. The concentrtion of totl solule mino cids in plnts sujected to inocultion ws higher only in tolernt plnts, if compred with sme tretments of plnts non-inoculted (Figure 7 A). Wter deficit promoted significnt increse in this vrile to ll tretments. The tolernt cultivr presented lower chnges, in comprison with sme tretments in sensitive cultivr. Totl solule proteins of inoculted plnts presented higher vlues (Figure 7 B), when compred to sme tretments in non-inoculted plnts. Wter deficit cused significnt decrese in oth cultivrs, presenting higher vrition in sensitive plnts. For proline the inoculted plnts presented higher vlues, compring with sme tretments in non-inoculted plnts (Figure 7 C). The two cultivrs demonstrted higher vlues in wter deficit, when compred with respective controls. These results present greter vrition in tolernt plnts, if compred with sme tretments in sensitive plnts. Tolernt plnts sumitted to inocultion presented significnt increse in mino cids, nd these results re ttriuted to iologicl fixtion of nitrogen. The nitrogense enzyme promotes the nitrogen sorption in form of nitrogen gs (N 2 ) nd conversion to mmonium (NH 4+ ). In ddition, the higher formtion of mino cids proly is linked to increse in ctivity of enzymes glutmine synthetse (GS), eing your ctivity depending of ATP (denosine-5'-triphosphte), nd glutmte synthse (GOGAT). In ddition, the increse in mino cids of plnts exposed to inocultion is due to greter flux nd etter ssimiltion of nitrogen in form of mmonium, concomitntly with higher ctivity of GS nd GOGAT enzymes. Rmos et l. [33] evluting the responses in Glycine mx plnts under wter deficit nd inocultion of Brdyrhizoium jponicum oserved lso n increse in concentrtion of totl solule mino cids. The concentrtion of totl solule mino cids in plnts under wter deficit incresed in ll tretments. This increment occurred proly due to increse in ctivity of protese enzymes, responsile y rekdown of proteins iming to djust osmoticlly the plnt [34]. Similr results on increse in mino cids were otined to Cost et l. [35] investigting Vign unguicult plnts. Delfini et l. [36] evluting the responses of two Archis hypoge cultivrs sumitted to inocultion of Brdyrhizoium sp. showed significnt increse in mino cids.

10 Tolernce to Drought in Leguminous Plnts Medited y Rhizoium nd Brdyrhizoium 57 Totl solule mino cids (µmol g DM -1 ) wter deficit c cd control c cd A 0 Totl solule proteins (mg g DM -1 ) c dc B C Proline (µmol g DM -1 ) d c d ce d ce 2 0 tolernt sensitive tolernt sensitive inoculted non-inoculted Figure 7. Totl solule mino cids (A), totl solule proteins (B), nd proline (C) in two contrsting Vign unguicult plnts under wter deficit nd sujected to inocultion. Mens followed y the sme letter re not significntly different y the Scott-Knott test t 5% of proility. The rs represent the men stndrd error [32]. The increse showed in totl solule proteins induced y inocultion suggests tht cteri ction resulted in increse in nitrogen supply through secondry route, tht is regulted y the nitrogense [37], ecuse in this study ws not verified increse in ctivity of the nitrte reductse fter inocultion. Hristozkov et l. [38] evluting the responses

11 58 Responses of Orgnisms to Wter Stress in Pisum stivum plnts under inocultion nd molydenum ppliction lso otined increse in protein levels. The decrese in protein levels promoted y the wter deficit is ssocited to decrese of the protein synthesis comined with increse of proteolytic enzymes, responsile y rekdown of solule proteins in plnts [39]. Cost [40] otined similr results studying Vign unguicult sujected to wter deficit, corroorting these results. The increse of proline levels provoked y the inocultion is proly linked to etter mino cids utiliztion such s glutmic cid nd rginine, eing the glutmic cid the precursor of the proline, while rginine cn suffer rection medited y enzyme clled of pyrrolline-5- croxylte reductse (P5CR) nd consequently to lierte proline [33]. Kohl et l. [41] lso oserved higher mounts of proline in Glycine mx plnts inoculted with Brdyrhizoium jponicum, contriuting with results of this study. The increse of proline in plnts under wter deficit is response to loss of cell turgescence [42]. Nogueir et l. [43] descrie tht the proline ccumultion hs een relted with drought tolernce in higher plnts, ctuting s osmoregultor gent with the ojective to keep wter in plnt tissue [44]. Similr ehvior ws descried y González et l. [45] working with Pisum stivum plnts under wter restriction. 6. Brdyrhizoium producing etter performnce on morphologicl prmeters Beneficil effects proportioned y the inocultion on growth prmeters re lrgely explored in crops s Phseolus vulgris nd Glycine mx, ut informtions on dry mtter ccumultion of Vign unguicult under wter deficit is limited. Bros et l. [32] conduced n experiment with 2 cultivrs (tolernt nd sensitive) comined with 2 wter regimes (wter deficit nd control), nd 2 inocultion forms (inoculted nd non-inoculted), totlizing 8 tretments. In shoot dry mtter the inocultion provoked increse, considering sme tretments in plnts non-inoculted (Figure 8 A). However, this increse only ws significnt in tolernt cultivr under inocultion nd irrigtion. Wter deficit occsioned significnt decrese in shoot dry mtter, with exception in tolernt cultivr non-inoculted. The tolernt plnts presented etter results, if compred with sensitive plnts independently of tretment (Figure 8 A). The inocultion provoked increse in plnt dry mtter, with exception in sensitive cultivr under irrigtion (Figure 8 B), compring to sme tretments in plnts non-inoculted. Wter deficiency induced decrese in plnt dry mtter for ll tretments, eing these significnt results when compred with control plnts. Independently of tretments ws showed tht sensitive cultivrs presented lower vlues, if compred to tolernt cultivrs.

12 Tolernce to Drought in Leguminous Plnts Medited y Rhizoium nd Brdyrhizoium wter deficit control A Shoot dry mtter (g) cd c dc c B Lef (numer) Plnt dry mtter (g) e d dc c dc c ed cd C c 0 tolernt sensitive tolernt sensitive inoculted non-inoculted Figure 8. Shoot dry mtter (A), plnt dry mtter (B), numer of leves (C) in two contrsting Vign unguicult plnts under wter deficit nd sujected to inocultion. Mens followed y the sme letter re not significntly different y the Scott-Knott test t 5% of proility. The rs represent the men stndrd error [32]. For lef numer occurred increse fter inocultion, with exception in sensitive plnts under wter deficiency (Figure 8 C). Wter deficit proportioned decrese in vlues of lef numer, eing significnt in comprison with control plnts. In tolernt cultivr were otined higher vlues of lef numer, if compred with sensitive cultivr.

13 60 Responses of Orgnisms to Wter Stress Shoot dry mtter ws mximized fter the inocultion procedure, eing this fct linked to proly increse in nodule numer in root (dt not shown), s well s it proportioned higher sorption nd vilility of nitrogen to plnt [46-47]. Similr results linked to shoot dry mtter were found y Figueiredo et l. [24] in reserch with Vign unguicult plnts exposed to inocultion of Brdyrhizoium. The wter deficit reduced the production of shoot dry mtter, with these effects ssocited to negtive interference of wter deficiency on iochemicl processes s nitrte ssimiltion nd iologicl fixtion of nitrogen [35], modifying indirectly the prtitioning of photo-ssimiltes in root nd shoot, nd consequent decrese in ccumultion of shoot iomss [48]. Similr results were found y Mendes et l. [49] working with two Vign unguicult cultivrs sumitted to drought during two stges. The inocultion proportioned increse of totl dry mtter, nd this result must e linked to etter development nd efficiency of root system, in which presents higher nitrogen sorption using the nodultion process. I ddition, normlly the higher nitrogen fixtion will produce increse in mino cids nd lso proteins [36], nd it exercises influence on photossimiltes vilility. Similr responses were descried y Sssi et l. [50] investigting two Phseolus vulgris cultivrs sujected to inocultion with cteri of Rhizoium gender. Plnts under wter deficiency frequently hve the production of dry mtter reduced, eing this decrese relted to fct tht wter deficit ffects severl metolic processes such s sorption of wter nd nutrients, which re fundmentl to keep dequte growth nd development rtes. Nscimento [51] lso reported tht wter deprivtion ffects the osmotic mechnism, nd y consequence reduces the CO 2 supply, tht is essentil in photosynthetic process. Similr results were found y Leite nd Virgens Filho [52] studying Vign unguiculd plnts exposed to wter deficit. The increse in lef numer promoted y inocultion is occsioned y the higher numer of nodules in root, nd consequently due to the etter iologicl fixtion of nitrogen [53]. Arújo et l. [54] studying Vign unguicult nd Leucen leucocephl plnts lso reported n increse of this vrile, confirming the results otined in this work. The lower lef numer fter wter deficiency is cused y the process of lef scission, nd this fct occurs due to sustrte not to present wter nd nutrient sufficient to supply the plnt exigencies [4]. Correi nd Nogueir [55] otined similr results with Archis hypoge plnts under wter deficit. 7. Finl considertions This chpter ws structured with recent informtions on cpcity of Brdyrhizoium nd Rhizoium to medite tolernce in leguminous plnts sumitted to wter deficit, which it cn e used y students, techers, reserchers, scientists nd frmers. It reveled concepts, effects, nd results on wter deficiency nd your consequences on plnts, s well s explored sever

14 Tolernce to Drought in Leguminous Plnts Medited y Rhizoium nd Brdyrhizoium 61 l possiilities linked to symiosis etween plnt-microorgnisms. Additionlly, it presented essentil compounds such s molydenum nd rections during process of iologicl fixtion of nitrogen. Also ws demonstrted the wter mintennce in lef nd nodule produced fter inocultion. Bsed in novel results, were relted interference positives on nitrogen compounds such s totl solule mino cids, proline, nd totl solule proteins. Other results prove the eneficil repercussion produced y inocultion with Brdyrhizoium on morphologicl prmeters. Acknowledgements This chpter hd finncil support from Conselho Ncionl de Pesquis (CNPq/Brzil) nd Coordenção de Aperfeiçomento de Pessol de Nível Superior (CAPES/Brzil) for Loto AKS. Author detils Alln Klynger d Silv Loto 1, Joquim Alenísio Gomes d Silveir 2, Roerto Cezr Loo d Cost 1 nd Cândido Ferreir de Oliveir Neto 1 1 Núcleo de Pesquis Vegetl Básic e Aplicd, Universidde Federl Rurl d Amzôni, Prgomins, Brzil 2 Lortório de Metolismo e Estresse de Plnts, Universidde Federl do Cerá, Fortlez, Brzil References [1] Rockström J, Flkenmrk M. Semirid crop production from hydrologicl perspective: Gp etween potentil nd ctul yield. Crit. Rev. Plnt Sci 2000; [2] Krmer PJ, Boyer JS. Wter reltions of plnt nd soils. Acdemic Press, New York [3] Fontn DC, Berlto MA, Bergmschi H. Micrometeorologicl ltertions in soyens grown under different wter regimes. Pesquis Agropecuári Brsileir 1992; [4] Sntos RF, Crlesso R. Wter deficit nd morphologic nd physiologic ehvior of plnts. Revist Brsileir de Engenhri Agrícol e Amientl 1998;

15 62 Responses of Orgnisms to Wter Stress [5] Cost RCL, Loto AKS, Silveir JAG, Lughinghouse HD. ABA-medited proline synthesis in cowpe leves exposed to wter deficiency nd rehydrtion. Turkish Journl of Agriculture nd Forestry 2011; [6] Shrp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT. Root growth mintennce during wter deficits: Physiology to functionl genomics. Journl of Experimentl Botny 2004; [7] Shrp RE, Silk WK, Hsio TC. Growth of the mize primry root t low wter potentils. I. Sptil distriution of expnsive growth. Plnt Physiology 1988; [8] Alino UB, Cmpo RJ. Effect of sources nd levels of molydenum on Brdyrhizoium survivl nd on iologicl nitrogen fixtion in soyen. Pesquis Agropecuári Brsileir 2001; [9] Mercnte MM, Gol SR, Frnco AA. Importnce of phenolics compounds in the interctions etween leguminous species nd rhizoi. Ciêncis d Vid 2002; [10] Bordeleu LM, Prevost D. Nodultion nd nitrogen fixtion in extreme environments. Plnt Soil 1994; [11] Squrtini A, Dzzo FB, Csell S, Nuti MP. The root-nodule symiosis etween Rhizoium hedysri nd its drought-tolernt host Hedysrum coronrium. Symiosis 1993; [12] Pu RN, Lwson DM. Trnsport, homeostsis, regultion, nd inding of molydte nd tungstte to proteins. Metl Ions in Biologicl Systems 2002; [13] Lwson DM, Smith BE. Molydenum nitrogenses: crystllogrphic nd mechnistic view. Metl Ions in Biologicl Systems 2002; [14] Bedmr EJ, Roles EF, Delgdo MJ. The complete dentrifiction pthwy of symiotic N-fixing cteri Brdyrhizoium jponicum. Biochemicl Society Trnsctions 2005; [15] Delgdo MJ, Bonnrd N, Tresierr-Ayl A, Bedmr EJ, Müller P. The Brdyrhizoium jponicum npedabc genes encoding the periplsmic nitrte reductse re essentil for nitrte respirtion. Microiology 2003; [16] Dixon R, Khn D. Genetic regultion of iologicl nitrogen fixtion. Nture Reviews Microiology 2004; [17] Loto AKS, Cost RCL, Oliveir Neto CF, Sntos Filho BG, Alves GAR, Freits JMN, Cruz FJR, Mrochio CA, Coimr GK. Responses of the pigments nd cron metolism in Vign unguicult cultivrs sumitted to wter deficit. Reserch Journl of Biologicl Sciences 2009; [18] Loto AKS, Oliveir Neto CF, Cost RCL, Sntos Filho BG, Cruz FJR, Lughinghouse IV HD. Biochemicl nd physiologicl ehviour of Vign unguicult (L.) Wlp. under wter stress during the vegettive phse. Asin Journl of Plnt Science 2008;

16 Tolernce to Drought in Leguminous Plnts Medited y Rhizoium nd Brdyrhizoium 63 [19] Sssi S, Aydi S, Gonzlez EM, Arrese-Tgor C, Adelly C. Understnding osmotic stress tolernce in leves nd nodules of two Phseolus vulgris cultivrs with contrsting drought tolernce. Symiosis 2010; [20] Bjji M, Lutts S, Kinet JM. Physiologicl chnges fter exposure to nd recovery from polyethylene glycol-induced wter deficit in cllus culture issued from durum whet (Triticum durum) cultivrs differing in drought resistnce. Journl of Plnt Physiology 2000; [21] Sssi AS, Aydi S, Gonzlez EM, Adelly C. Osmotic stress ffects wter reltions, growth, nd nitrogen fixtion in Phseolus vulgris plnts. Act Physiologie Plntrum 2008; [22] Sprent JJ. Nitrogen fixtion. In Physiology nd Biochemistry of drought resistnce in plnts. Eds. L C Pleg nd D Aspinll. pp Acdemic Press [23] Venkteswrlu B, Neelm S, Mheswri M Nodultion nd N 2 (C 2 H 2 ) fixtion in cowpe nd groundnut during wter stress nd recovery. Field Crops Reserch 1990; [24] Figueiredo MVB, Vilr JJ, Burity HA, Frnç FP. Allevition of wter stress effects in cowpe y Brdyrhizoium ssp. Inocultion. Plnt nd Soil 1999; [25] Alves JMA, Arújo NP, Uchô SCP, Aluquerque JAA, Silv AJ, Rodrigues GS, Silv DCO. The groeconomic evlution of the production of cowpe vrieties intercropped with vrieties of cssv in The Stte of Rorim. Revist Agromiente 2009; [26] Frot KMG, Sores RAM, Arês JAG. Chemicl composition of cowpe [Vign unguicult (L.) Wlp], BRS-Milênio cultivr. Ciênci e Tecnologi de Alimentos 2008; [27] Oliveir AP, Sorinho JT, Nscimento JT, Alves AU, Aluquerque IC, Bruno GB. Evlution of reeding lines nd cultivrs of cowpe-ens in Arei, Pri, Brzil. Horticultur Brsileir 2002; [28] Rmos MLG, Gordon AJ, Minchin FR, Sprent JI, Prsons R. Effect of wter stress on nodule physiology nd iochemistry of drought tolernt cultivr of common en (Phseolus vulgris L.). Annls of Botny 1999; [29] Silveir JAG, Mtos JCS, Cectto VM, Viegs RA, Oliveir JTA. Nitrte reductse ctivity, distriution, nd response to nitrte contrsting Phseolus species inoculted with Rhizoium spp. Environment nd Experimentl Botny 2001; [30] Mores WB, Mrtins Filho S, Grci SGO, Cetno SP, Mores WB, Cosmi FC. Evlution of iologicl, fixtion of nitrogen in rhizoium under wter deficit. Idesi 2010; [31] Serrj R, Sinclir TR. Processes contriuting to N 2 fixtion insensitivity to drought in the soyen cultivr Jckson. Crop Science 1996;

17 64 Responses of Orgnisms to Wter Stress [32] Bros MAM, Loto AKS, Vin GDM, Coelho KNN, Bros JRS, Mores MCHS, Cost RCL, Sntos Filho BG, Oliveir Neto CF. Reltionship etween totl solule proteins nd dry mtter in two contrsting cowpe cultivrs induced to inocultion nd wter deficiency. The Scientific World Journl, 2012;pper is press. [33] Rmos MLG, Prsons R, Sprent JI. Differences in ureide nd mino cid content of wter stressed soyen inoculted with Brdyrhizoium jponicum nd B. elknii. Pesquis Agropecuári Brsileir 2005; [34] Cost RCL, Loto AKS, Oliveir Neto CF. Vrition in content of totl solule mino cids in leves of cowpe under wter stress. In: Congresso Ncionl de feijão cupi, pp. 1-19, Teresin, PI, mio, [35] Cost RCL, Crdoso BB, Silv JT, Gomes Filho JGF, J. A. G. Silveir JAG. Wter stress strongly decreses the ssimiltion of nitrte nd nodultion in cowpe (Vign unguicult, (L.) Wlp.). In Reunião Ncionl de Pesquis de Cupi, pp , Teresin, PI, Brzil, mrch, [36] Delfini R, Belgoff C, Fernández E, Fr A, Cstro S. Symiotic nitrogen fixtion nd nitrte reduction in two penut cultivrs with different growth hit nd rnching pttern structures. Plnt Growth Regultion 2010; [37] Mrschner H, Minerl nutrition of higher plnts, Acdemic Press, pp. 889, London, UK, [38] Hristozkov M, Genev M, Stnchev I, Response of inoculted pe plnts (Pisum stivum L.) to root folir fertilizer ppliction with reduced molydenum concentrtion. Plnt Physiology 2006; [39] Lechinoski A, Freits JMN, Cstro DS, Loto AKS, Oliveir Neto CF, Cunh RLM. Influence of wter stress on levels of solule mino cids nd proteins in leves of tek (Tecton grndis L. f.). Revist Brsileir de Biociênci 2007; [40] Cost RCL. Nitrogen ssimiltion nd osmotic djustment in plnts nodulted ento-string Vign unguicult (L.) Wlp. Sujected to wter stress. Ph.D Thesis. Universidde Federl do Cerá, Brsil, [41] Kohl DH, Kennelly DJ, Zhy Y, Schuert KR, Sheder G. Proline ccumultion, nitrogense (C 2 H 2 reducing) ctivity nd ctivities of enzymes relted to proline metolism in drought-stressed soyen nodules. Journl of Experimentl Botny 1991; [42] Oliveir AAO, Brreto LP, Bezerr Neto E, Sntos MVF, Cost JCA. Orgnic solutes in forge sorghum genotypes under slt stress. Pesquis Agropecuári Brsileir 2006; [43] Nogueir RJMC, Sntos CR, Neto EB, Sntos VF. Physiologicl ehviour of two penut cultivrs sumitted to suppression wtering. Pesquis Agropecuári Brsileir 1998;

18 Tolernce to Drought in Leguminous Plnts Medited y Rhizoium nd Brdyrhizoium 65 [44] Muchow RC, Crerry PS. Designing improved plnt types for the semi-rids tropics: Agronomist` viewpoints. In: penning de vries, F.W.T. Teng, P. Metselr, Eds., Dordrecht:Kluwer, pp , Merylnd, EUA, [45] González EM, Apricio-Tejo PM, Gordon AJ, Minchin FR, Igor CA. Wter-deficit effects on cron nd nitrogen metolism of pe nodules. Journl of experimentl Botny 1998; [46] Epstein E, Bloom AJ. Nutrition nd growth. In: E. Epstein nd A. J. Bloom, Ed. pp , Londrin, PR, Brzil, [47] Souz RA, Hungri M, Frnchini JC, Mciel CD, Cmpo RJ, Zi DAM. Miniml set of prmeters for evlution soil microiot nd iologicl nitrogen fixtion in soyen. Pesquis Agropecuári Brsileir 2008; [48] Correi GK, Nogueir CMJR. Evlution of the growth of groundnut (Archis hypoge L.) sujected to wter deficit. Revist de Biologi e Ciêncis d Terr 2004; [49] Mendes RMS, Távor FJAF, Pitomeir JB, Nogueir RJMC. Source-sink reltionships in cowpe under drought stress. Revist Ciênci Agronômic 2007; [50] Sssi S, Aydi S, Gonzlez EM, Arrese-Tgor C, Adelly C. Understnding osmotic stress tolernce in leves nd nodules of two Phseolus vulgris cultivrs with contrsting drought tolernce. Symiosis 2010; [51] Nscimento SP. Effect of wter deficit in cowpe to identify genotypes with drought tolernce. Ph.D Thesis, Universidde Federl do Piuí, [52] Leite ML, Virgens Filho JS. Dry mtter production of cowpe [Vign unguicult (L.) Wlp] plnts sumitted to wter deficits. Exts Terr 2004; [53] Ferreir EPB, Mrtins LMV, Xvier GR, Rumjnek NG. Nodultion nd grin yield y cowpe [Vign unguicult (L.) Wlp.] Inoculted with rhizoi, isoltes. Revist Cting 2011; [54] Arújo ASF, Crneiro RFV, Bezerr AAC, Arújo FF. Co-inocultion Rhizoi nd Bcilus sutilis in cowpe nd Leucen: effects on nodultion, N 2 fixtion nd plnt growth. Ciênci Rurl 2009; [55] Correi KG, Nogueir RJMO. Assessment of growth of penut (Archis hypoge L.) sujected wter deficit. Revist de Biologi e Ciênci d Terr 2004;

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