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Differential Expression of the TFIIIA RegulatoryPathway in Response to Salt Stress between
 Medicago truncatula
Genotypes
1[W]
Laura de Lorenzo, Francisco Merchan, Sandrine Blanchet, Manuel Megı´as, Florian Frugier,Martin Crespi*, and Carolina Sousa
Institut des Sciences du Ve´ge´tal, Centre National de la Recherche Scientifique, F–91198 Gif-sur-Yvette cedex,France (L.d.L., F.M., S.B., F.F., M.C.); and Departamento de Microbiologı´a y Parasitologı´a, Facultad deFarmacia, Universidad de Sevilla, 41012 Seville, Spain (L.d.L., F.M., M.M., C.S.)
Soil salinity is one of the most significant abiotic stresses for crop plants, including legumes. These plants can establish rootsymbioses with nitrogen-fixing soil bacteria and are able to grow in nitrogen-poor soils.
Medicago truncatula
varieties showdiverse adaptive responses to environmental conditions, such as saline soils. We have compared the differential root growth of two genotypes of 
M. truncatula
(108-R and Jemalong A17) in response to salt stress. Jemalong A17 is more tolerant to salt stressthan 108-R, regarding both root and nodulation responses independently of the nitrogen status of the media. A dedicatedmacroarray containing 384 genes linked to stress responses was used to compare root gene expression during salt stress inthese genotypes. Several genes potentially associated with the contrasting cellular responses of these plants to salt stress wereidentified as expressed in the more tolerant genotype even in the absence of stress. Among them, a homolog of the abioticstress-related
COLD
-
REGULATEDA1
gene and a TFIIIA-related transcription factor (TF), MtZpt2-1, known to regulate theformer gene. Two MtZpt2 TFs (MtZpt2-1 and MtZpt2-2) were found in Jemalong A17 plants and showed increased expressionin roots when compared to 108-R. Overexpression of these TFs in the sensitive genotype 108-R, but not in Jemalong A17, led toincreased root growth under salt stress, suggesting a role for this pathway in the adaptive response to salt stress of these
M.truncatula
genotypes.
Maintaining crop yields under adverse stress envi-ronmental conditions is a major challenge in modernagriculture. To meet this goal, it is necessary to under-stand the contrasting adaptations of plants to growthin stressed conditions. Salinity is one of the majorabiotic stresses that affects crop productivity andquality and has been described as one of the mostserious threats to agriculture and the natural status of the environment (Chinnusamy et al., 2005). Increasedsalinization of arable land is expected to have devas-tating global effects,resultingin a30% land loss withinthe next 25 years and up to 50% by the year 2050(Wang et al., 2003).Plant responses to salt stress are diverse and includemodifications of root system architecture, activationof stress-induced transcriptional programs, and bio-chemical adaptations, as well as plant growth inhibi-tion. Salinity imposes ionic, osmotic, and secondarystresses, such as nutritional disorders and oxidativestress (Zhu, 2001). Legumes, like most crop plants, aresusceptible to salinity (Duzan et al., 2004; Chinnusamyet al., 2005). These plants are widely grown for grainand forage purposes, their world-wide economic im-portance being second only to grasses (Graham andVance, 2003). In addition, legumes can establish rootsymbioses with nitrogen-fixing soil bacteria, enablingtheplantstogrowinnitrogen-poor soils. This ability tocolonize soils where other plants cannot thrive makesthe study of legumes and their symbioses importantfor agriculture. The establishment of successful sym- biosis involves an elaborate exchange of molecularsignals (Limpens and Bisseling, 2003). In the planthost, root nodule organogenesis is regulated by di-verse hormonal, metabolic, and environmental condi-tions (Crespi and Ga´lvez, 2000), and this interaction isspecifically affected in saline soils (Arrese-Igor et al.,1999; Zahran, 1999).The problem of salinity has been approachedthrough better management practices and the intro-duction of salt-tolerant varieties in the affected areas.Unfortunately, these approaches are generally uneco-nomical and difficult to implement on a large scale.However, major progress could be achieved throughgenetic improvement (Walia et al., 2005). Various le-gumes, such as the model legume
Medicago truncatula
,show a large diversity of varieties adapted to vary-ing environmental conditions, including saline soils
1
This work was supported by the Spanish Department of Edu-cation and Science (a university professor training grant to L.d.L.and a postdoctoral grant to F.M.), and by the ‘‘Grain Legumes’’ FP6European Economic Community project.* Corresponding author; e-mail crespi@isv.cnrs-gif.fr.The author responsible for distribution of material integral to thefindings presented in this article in accord with the policy describedin the Instructions for Authors (www.plantphysiol.org) is: MartinCrespi (crespi@isv.cnrs-gif.fr).
[W]
The online version of this article contains Web-only data.www.plantphysiol.org/cgi/doi/10.1104/pp.107.106146
Plant Physiology,
December 2007, Vol. 145, pp. 1521–1532, www.plantphysiol.org
Ó
2007 American Society of Plant Biologists 1521
 
(http://www.noble.org/medicago/ecotypes.html). Inrecent years,
M. truncatula
has been recognized as anexcellent legume model in view of its small, diploid ge-nome, self fertility, and short life cycle, as well as avail-ability of various genomic and genetic tools (Barkeret al., 1990; Bell et al., 2001; Young et al., 2005). All thesetraits make
M. truncatula
suitable for identifying genesthat could improve agronomic performances such asabiotic stress resistance (Cook, 1999).Stress responses involve alterations in gene expres-sion (Tester and Davenport, 2003), suppressive sub-tractive hybridizations, and array technologies usingcDNAs or oligonucleotides are increasingly beingused to monitor global gene expression changes invarious plants in response to abiotic stresses (Ozturket al., 2002; Seki et al., 2002; Bartels and Sunkar, 2005).However, few reports analyzed differences in geneexpression between salt-sensitive and salt-tolerantgenotypes in plants (Walia et al., 2005). Althoughsuch genes are useful in the dissection of genotype-specific regulatory pathways and mechanisms of salttolerance, they usually represent only a fraction of allsalt-regulated genes, and isolating them is a challeng-ing task. The mechanisms underlying the genotype-dependent difference in expression of such genes arelargely unknown.Two genotypes (108-R and Jemalong A17) wereshown to have a different adaptation to salt stress(Merchan et al., 2003). We have developed, in the
M.truncatula
108-R genotype, a dedicated macroarraycontaining genes linked to salt stress and recoveryresponses in roots (Merchan et al., 2007). Here, weaimed to identify genes involved in genotype-specificregulatory pathways and mechanisms of salt acclima-tion. A comparison of molecular and physiologicalresponses to salt stress in sensitive and tolerant
M.truncatula
genotypes (108-R and Jemalong A17, re-spectively) was performed. Expression analysis usingthe dedicated macroarray revealed several genes po-tentially associated with the contrasting responses tosalt stress in these plants. Among them, we identifieda homolog of the
COLD
-
REGULATEDA1
(
CorA1
;
 MtCorA1
;Labergeetal.,1993)gene,whichisaputativetarget of MtZpt2 transcription factors (TFs; Merchanet al., 2007). Accordingly, these TFs showed higher ex-pression levels in the tolerant variety. Overexpressionof 
MtZpt2
-
1
or
MtZpt2
-
2
in roots of the salt-sensitivevariety allowed significant increase in root growthspecifically under salt stress conditions, suggesting arole of these pathways in the differential adaptiveresponse to salt stress of these
M. truncatula
genotypes.
RESULTSEvaluation of Salt Stress Growth Responses of Two
 M. truncatula
Genotypes
We have examined root growth and dry weight biomass in two genotypes of the model legume
 M. truncatula
(108-R and Jemalong A17) in responseto different salt stress conditions. Root length wasmeasured after 5 d of growth on a rich medium(Fahra¨eus; Truchet et al., 1985) containing variousconcentrations of NaCl (Fig. 1). Root length of 
M.truncatula
108-R was significantly reduced after NaCltreatments in the range of 90 to 150 m
M
, as comparedwith plants grown without salt (Kruskal and Wallistest,
P
,
0.01;
n
5
20; Fig. 1A). However, root length in Jemalong A17 was negatively affected by salinity onlyat 150 m
M
(Kruskal and Wallis test,
P
,
0.01;
n
5
20;Fig. 1A). Altogether, we could identify a differentialresponse to salt stressbetween the 108-R and JemalongA17 genotypes. As shown in Figure 1B,
M. truncatula
 Jemalong A17 grewwellathigh salinitylevels (120 m
M
NaCl), while 108-R plants grew more slowly underthese salt conditions. Similarly, salt treatment re-duced the root dry weight more noticeably for thevariety 108-R already after a 60 m
M
NaCl treatment,whereas it was only significantly affected at 150 m
M
in Jemalong A17 (Kruskal and Wallis test,
P
,
0.01;
n
5
20; Fig. 1C, left). No significant differences were,however, found for leaf dry weight biomass of eachvariety and in all treatments, suggesting greater saltsensitivity of the root than of the aerial part at thisearly postgermination stage (Fig. 1C, middle). Theratio of root dry weight to leaf dry weight (as per-centage of control) reveals the relative effects of increasing NaCl concentration for each genotype(Fig. 1C, right). As expected, ratio values for
M.truncatula
108-R were significantly reduced with in-creased salt treatments (60–150 m
M
NaCl; Kruskaland Wallis test,
P
,
0.01;
n
5
20). In contrast, this ratiowas constant for the tolerant genotype, at least up to120 m
M
NaCl. These results suggest that root dryweight is significantly different between the twogenotypes at medium and high salt concentrations(60–150 m
M
).Root growth performance was also assessed on alow-nitrogen medium (‘‘i’’; Blondon, 1964) to exam-ine the impact of the medium on the range of vari-ability for salinity tolerance between these twogenotypes of 
M. truncatula
. At the same salinityconcentration, root length of 108-R was even moresignificantly affected by salt treatment when com-pared with the results obtained in the rich medium.This difference is likely to be a consequence of min-imal nutrient capacity of the ‘‘i’’ medium that maypotentiate salt stress effects on growth. Statisticallysignificant differences between 108-R and JemalongA17 genotypes were found for all assayed salinityconditions (Fig. 1D).
M. truncatula
108-R growth wasalready reduced by more than 50% at 90 m
M
of salt,and an NaCl concentration of 150 m
M
nearly abol-ished root growth. This negative effect of salt on rootgrowthwaslesspronouncedinJemalongA17,inagree-ment with the results obtained on rich (Fahra¨eus)medium (Fig. 1A).These various parameters allowed us to monitor theeffects of salt treatments on plant growth and furtherrevealed differential root growth responses between
de Lorenzo et al.1522 Plant Physiol. Vol. 145, 2007
 
Figure 1.
EffectofNaClonrootgrowth anddry weightoftwo
M.truncatula
genotypes. Rootlengthanddry weightbiomassunderdifferent salt stress conditions were evaluated in an in vitro system. Germinated seedlings were grown on vertical Fahra¨eus or ‘‘i’’medium plates for 5 d inthe presence ofdifferent NaClconcentrations (0, 30, 60, 90, 120,and 150 m
M
).A,Relative root lengthof each variety at 5 d.a.g. in in vitro conditions with Fahra¨eus medium is shown as percentage of control root growth without salt. B,Representative pictures taken 5 d after transfer of the seedlings to 0, 30, and 120 m
M
NaCl on Fahra¨eus medium. C, Relative dry
Differential Salt Stress Responses in LegumePlant Physiol. Vol. 145, 2007 1523
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