Plant molecular stress responses face climate change

Supplementary Material

Plant molecular stress responses face climate change Ishita Ahuja1, 2, Ric C. H. de Vos2, 3, Atle M. Bones1 and Robert D. Hall2, 3, 4 1

Department of Biology, Norwegian University of Science and Technology, Realfagbygget, NO-7491 Trondheim, Norway 2 Plant Research International, P.O. Box 16, 6700 AA Wageningen, The Netherlands 3 Centre for BioSystems Genomics, P.O. Box 98, 6700AB Wageningen, The Netherlands. 4 Netherlands Metabolomics Centre, Einsteinweg 55, 2333 CC Leiden, The Netherlands

Corresponding author: Hall, R.D. ([email protected])

Table S1. Abbreviations and description of the genes, proteins and enzymes involved in different environmental stress factors (ESFs) Gene/Protein/ Enzyme

Plant

ESFs

Description and molecular mechanisms (known/putative)

Refs

ABAR

Drought

At1g80160

Arabidopsis

Drought

At3g53990 At3g55940 At4g36010 ABI1 ATHB-7

Arabidopsis Arabidopsis Arabidopsis Arabidopsis Arabidopsis

Drought Drought Drought Drought Multiple

BhHsf1 (Figure 1, c3)

Boea hygrometrica

Elevated temperature

BiP

Arabidopsis

Drought

BOB1(Figure 1, c5)

Arabidopsis


Abscisic acid (ABA)-related gene / ABA-binding protein; encodes magnesium chelatase that is involved in plastid-to-nucleus signal transduction Genes represents subgroups I and II of transcription factors with an APETELA2 (AP2) domain Putative Galactinol synthase (GolS3) Putative AP2 domain-containing DNA binding protein, Dehydrin xero2 (XERO2) / low temperature–induced protein (LTI30) Late embryogenesis-abundant protein, putative Galactinol synthase, putative (GolS2) Proton-dependent oligopeptide transport (POT) family protein / Nitrate transporter 1.7 Encodes a lactoylglutathione lyase family protein / glyoxalase I family protein Universal stress protein (USP) family protein Phosphoinositide-specific phospholipase C, putative Pathogenesis-related thaumatin family protein ABA insensitive 1 A. thaliana homeobox 7; encodes a putative transcription factor that contains a homeodomain closely linked to a leucine zipper motif, regulates in an ABA-dependent manner and may act in a signal transduction pathway which mediates a drought response An Hsf from the resurrection plant B. hygrometrica; may play dual roles in mediating heat tolerance and growth retardation via regulation of target genes related to stress response and mitotic cell cycle Binding protein; chaperone protein, play crucial roles in assisting protein folding during endoplasmic reticulum (ER) stress, which can result from N-glycosylation defects BOBBER1; A NudC domain containing Arabidopsis small heat shock protein; required for the normal partitioning and patterning of the apical domain of the Arabidopsis embryo, first time evidenced to have both developmental and thermotolerance functions, and may play a role in

[S1–S2]

At1g09350 At1g22985 At3g50970 At1g52690 At1g56600 At1g69870

Arabidopsis (Arabidopsis thaliana) Rice (Oryza sativa) Arabidopsis Arabidopsis Arabidopsis Arabidopsis Arabidopsis Arabidopsis

AP37 and AP59

Multiple Drought Drought Drought Drought Drought Drought

[S3] [S4] [S5] [S4] [S5] [S4] [S2,S5] [S6] [S5] [S4] [S4] [S2,S7] [S2,S8]

[S9]

[S10]

[S11]

1

bZIP60

Arabidopsis

Drought

CBK3 (Figure 1, c1)

Arabidopsis

CcHyPRP

Pigeonpea (Cajanus cajan)

Elevated temperature Multiple

COR

Wheat (Triticum aestivum) Arabidopsis Arabidopsis

Multiple

Arabidopsis

Salinity

Wheat (Triticum durum) Arabidopsis

Drought

DRIP1 and DRIP2 (Figure 1, b3) DSM1

Arabidopsis

Drought

Rice

Drought

ERF

Arabidopsis

Multiple

FLC FTA (Figure 1, a4)

Arabidopsis Canola (Brassica napus)

Elevated CO2 Drought

FtsH11

Arabidopsis


GA2ox7 (Figure 1, d3) GH3 (Figure 1, a6) GmWRKY13, GmWRKY21 and GmWRKY54 G protein (Figure 1, a3)

Arabidopsis Arabidopsis Soybean (Glycine max)

Salinity Drought Multiple

Arabidopsis

GRP7

Arabidopsis

Elevated temperature and Drought Multiple

GSNOR

Arabidopsis

HKT1;1

Arabidopsis

Elevated temperature Salinity

HOS3

Arabidopsis

Multiple

HOT5

Arabidopsis

HPR1

Arabidopsis

Elevated temperature Drought

HSFA1a (Figure 1, c1)

Arabidopsis

HsfA3 (Figure 1, c6)

Arabidopsis

COR47 DDF1 (Figure 1, d3)

DELLA proteins (Figure 1, d3) DHN genes DREB2A (Figure 1, b1,2,3; c6)

Drought Salinity

Drought

Elevated temperature Elevated

both of these folding networks Basic domain/leucine zipper60; shown to activate BiP expression, probably through ER stress response element–like sequences Calmodulin-binding protein kinase 3; controls the binding activity of HSFs to HSEs by phosphorylation of AtHSFA1 A hybrid-proline-rich protein encoding gene; contains a repetitive proline-rich (PR) N-terminal domain and a conserved eight cysteine motif (8CM) at the C-terminus, shows multiple abiotic stress tolerance at cellular and whole plant levels Cold regulated gene

[S10] [S12] [S13]

[S14]

Cold-regulated 47; belongs to the dehydrin protein family Dwarf and delayed flowering 1; salinity-responsive gene encoding an AP2 transcription factor of the DREB1/CBF subfamily, causes dwarfism mainly by levels of reducing bioactive gibberellic acid (GA) in transgenic Arabidopsis Play a pivotal role in the negative regulation of GA signalling, probably as transcriptional regulators Dehydrin genes belong to family of LEA proteins

[S2,S10] [S15]

Dehydration-responsive element binding protein 2; encodes a transcription factor that specifically binds to DRE/CRT cis elements (responsive to drought and low-temperature stress) Encode DREB2A-interacting protein 1 and 2; C3HC4 RING domain– containing proteins that interact with the DREB2A protein in the nucleus A putative mitogen-activated protein kinase (MAPK) kinase kinase (MAPKKK); functions as an early signalling component in regulating responses to drought stress by regulating scavenging of reactive oxygen species (ROS) in rice Encodes a member of the DREB subfamily A-4 of ethylene response factor Flowering locus C; floral suppressor gene α-subunit of farnesyltransferase; involved in protein prenylation, regulates in response to ABA and drought, conditional and specific down-regulation of FTA in canola using the AtHPR1 promoter driving an RNAi construct resulted in yield protection against drought stress FtsH protease 11; Filamentous temperature sensitive H (FtsH) encodes a membrane-bound, ATP-dependent metalloprotease involved in regulation of the heat-shock transcription factor σ32. GA 2-oxidase 7; encodes a C20-GA deactivation enzyme Encode auxin-conjugating enzymes Soybean WRKY-type transcription factor genes; play differential roles in abiotic stress tolerance

[S2,S5]

[S15] [S16]

[S2,S17] [S18]

[S2,S8] [S19] [S20]

[S21]

[S15] [S21] [S22]

A heterotrimeric GTP-binding protein

[S7,S23]

Glycine-rich protein 7; seems to promote stomatal opening and reduce tolerance under salt and dehydration stress conditions, but promotes stomatal closing and thereby increases stress tolerance under conditions of cold tolerance S-nitrosoglutathione reductase, which metabolizes the Nitric oxide (NO) adduct S-nitrosoglutathione High affinity potassium transporter1; a plasma membrane protein expressed in the root stele, mediates salinity tolerance Hyper-osmotically sensitive gene with high homology to CIG30 (ELO2); controls very long chain fatty acids (VLCFA) composition and functions to inhibit ABA-mediated stress responses, including regulation of stomatal aperture. CIG30 has been implicated in synthesis of VLCFA, which are essential precursors for sphingolipids and ceramides. Sensitive to hot temperatures; encodes S-nitrosoglutathione reductase (GSNOR) Hydroxypyruvate reductase; since the promoter region contains the core motif of DREB2A, the expression is drought inducible Class A Heat Shock Factor 1A

[S2,S24]

[S2,S12]

Heat Shock Transcription Factor A3; HsfA3 is transcriptionally induced

[S2,S28]

2

[S25] [S26] [S27]

[S25] [S20]

temperature HvCBF4

Barley (Hordeum vulgare)

Multiple

InsP5-ptase (Figure 1, b2)

Arabidopsis

Drought

ISPS

Black poplar (Populus nigra)

Drought

ITN1 (Figure 1, d2)

Arabidopsis

Salinity

LEA

Wheat, Arabidopsis

Drought, Multiple

LEW1

Arabidopsis

Multiple

LOS2 (Figure 1, d5) LTP3 and LTP4

Arabidopsis Arabidopsis

Salinity Drought

miR169 (Figure 1, a1) MSI1 (Figure 1, a8)


Drought Drought

MT2A MYB96 (Figure 1, a6)


Drought Drought

NCED3

Arabidopsis

Multiple

NFYA5 (Figure 1, a1)

Arabidopsis

Drought

OCP3 (Figure 1, a7)

Arabidopsis

Drought

OsABF1

Rice

Multiple

OsDREB2A (Figure 1, d1)

Rice

Salinity

OsRMC (Figure 1, d1)

Rice

Salinity

PAO PFD3 and PFD5

Maize (Zea mays) Arabidopsis

Salinity Salinity

PIP2 (Figure 1, c2)

Arabidopsis

PIPK (Figure 1, c2)

Arabidopsis

PLD (Figure 1, c2)

Arabidopsis

Elevated temperature Elevated temperature Elevated

during heat stress by DREB2A, and HsfA3 in turn regulates the expression of Hsp-encoding genes Hordeum vulgare C-repeat binding factor 4; a barley orthologue of CBF/DREB, expression is induced by low temperature stress, CBF/DREBs of barley are suggested to act differently from those of Arabidopsis in transgenic rice over-expressing HvCBF4 Inositol polyphosphate 5-phosphatase; specifically hydrolyzes soluble inositol phosphates and terminates the signal, drought tolerance of the InsP5-ptase plants is mediated in part via a DREB2A-dependent pathway Isoprene synthase; catalyzes the synthesis of isoprene from dimethylallyl diphosphate in planta, isoprene (most abundant volatile organic compound) is considered to be an important molecule for ameliorating abiotic stresses Increased tolerance to NaCl1; encodes a transmembrane protein with an ankyrin-repeat motif that has been implicated in diverse cellular processes such as signal transduction Late embryogenesis abundant proteins; accumulate under stress conditions such as drought, salinity and low temperatures, but they are present also in ABA-treated vegetative plants Leaf Wilting 1; encodes a cis-prenyltransferase, catalyzes dolichol biosynthesis, which is important for plant responses to drought. Dolichols are long-chain unsaturated polyisoprenoids with multiple cellular functions, such as serving as lipid carriers of sugars used for protein glycosylation, which affects protein trafficking in the endoplasmic reticulum. Low expression of osmotically responsive genes 1 Lipid transfer protein 3 and Lipid transfer protein 4; LTP4 is strongly upregulated by ABA MicroRNA 169A; targets mRNAs for cleavage or translational repression A subunit of polycomb group protein complexes and chromatin assembly factor 1; can bind to the chromatin of the drought-inducible downstream target RD20, plays role in the negative regulation of the drought stress response Metallothionein protein, putative A R2R3-type MYB transcription factor; a molecular link mediating ABAauxin cross talk in drought stress response and lateral root growth, providing an adaptive strategy under drought stress conditions Nine-cis-epoxycarotenoid dioxygenase 3; a key enzyme of ABA biosynthesis, regulates in response to drought and salinity Nuclear factor Y A5; encodes a member of the CCAAT-binding transcription factor (CBF-B/NF-YA) family and contains a target site for miR169, up-regulated in response to ABA and drought A transcriptional regulator from the homeodomain (HD) family; proposed to have a regulatory role in the adaptive responses to drought tolerance and disease resistance to fungal pathogens, functioning as a modulator of independent and specific aspects of the ABA- and methyl jasmonate (MeJA)-mediated signal transduction pathways Oryza sativa ABA responsive element binding factor 1gene; encodes a bZIP transcription factor, expression in seedling shoots and roots was found to be induced by anoxia, salinity, drought, oxidative stress, cold and ABA Encode Oryza sativa Dehydration-responsive element-binding protein 2A Oryza sativa root meander curling; an apoplastic protein, with extracellular domain-like cysteine-rich motifs (DUF26) Polyamine oxidase Prefoldins 3 and 5; encode proteins orthologous to prefoldin (PFD) subunits 3 and 5 from yeast and mammals, involved in unfolded protein binding. Disruption of PFD3 and PFD5 provokes a hypersensitivity of Arabidopsis to elevated concentrations of NaCl that correlates with very low levels of α- and β-tubulin. Phosphatidylinositol 4,5-bisphosphate

[S29]

[S4]

[S30]

[S31]

[S8,S14,S16]

[S10]

[S2,S32] [S2,S6] [S33] [S2,S6]

[S5] [S21]

[S2,S8] [S2,S33]

[S34]

[S35]

[S36] [S36] [S37] [S38]

[S23]

Phosphatidylinositolphosphate kinase

[S23]

Phospholipase D

[S23]

3

temperature Drought

PLDα1 (Figure 1, a 2; a3)

POX22.3, POX8.1 PP2C (Figure 1, a3)

Rice Arabidopsis

PUB22 and PUB23 (Figure 1, b4)

Arabidopsis

Drought Drought, Multiple Drought

Rab16A (Figure 1, d1) RBOHC and RBOHD (Figure 1, d2) RCA

Rice Arabidopsis

Salinity Salinity

Arabidopsis

RCA1 (Figure 1, c4)

Arabidopsis

RD20

Arabidopsis

Elevated temperature Elevated temperature Drought

RD22 (Figure 1, a6; d2) RD29A and RD29B (Figure 1, d2)


Salinity Drought, Multiple

Rma1H1 (Figure 1, b5)

Hot pepper (Capsicum annuum) and Arabidopsis

Drought

ROF1

Arabidopsis


RPN12a (Figure 1, b4)

Arabidopsis

Drought

SAL1 (Figure 1, a5)

Arabidopsis

Drought

Ser 228 SODs

Arabidopsis Alfalfa (Medicago sativa) Archaeal hyperthermophile (Pyrococcus furiosus) Arabidopsis

Salinity Drought

SOR

SOS2

[S39]

[S18] [S2,S8]

Plant U-Box 22 and 23, encodes cytoplasmically localized U-box domain E3 ubiquitin ligases proteins that are involved in the response to water stress and acts as a negative regulator of PAMP-triggered immunity Rice salt responsive gene; belongs to the group 2 LEA gene family Respiratory burst oxidase homolog C and Respiratory burst oxidase homolog D; encode the ROS-producing NADPH oxidases Rubisco activase

[S2,S40]

[S36] [S2,S31] [S41]

43-kD b (short isoform) of RCA

[S41]

Responsive to desiccation 20; encodes a calcium binding protein whose mRNA is induced upon treatment with NaCl, ABA and in response to desiccation Responsive to desiccation 22 Responsive to desiccation 29A/Cold regulated 78 (COR78) and Responsive to desiccation 29B; RD29B is induced in expression in response to water deprivation such as cold, high-salt, and desiccation, response appears to be via ABA A hot pepper (Capsicum annuum) homolog of a human RING membrane-anchor 1 E3 ubiquitin ligase; play a critical role in the downregulation of plasma membrane aquaporin levels by inhibiting aquaporin trafficking to the plasma membrane and subsequent proteasomal degradation as a response to dehydration in transgenic Arabidopsis plants Rotmase FKBP 1; A peptidyl prolyl cis/trans isomerase and a member of the FKBP (FK506 binding protein) family; exposure to heat stress induces nuclear localization of the ROF1–HSP90.1 complex, which is dependent upon the presence of the transcription factor HsfA2, which interacts with HSP90.1 but not with ROF1 Regulatory particle non-ATPase 12a; encoding a non-ATPase subunit of the 26S proteasome complex, together with other non-ATPase subunits forms the lid sub- complex, which functions in substrate recognitioin and processing before Ub-tagged proteins enter into the core particle Encodes a bifunctional protein that has 3'(2'),5'-bisphosphate nucleotidase and inositol polyphosphate 1-phosphatase activities with alx8 (altered expression of APX2) mutation. alx8 mutant has constitutively increased ABA content, higher expression of genes responsive to high light stress and is reported to be drought tolerant. An autophosphorylation site of the protein kinase SOS2 Superoxide dismutases

[S2,S6]

[S45] [S46]


Superoxide reductase

[S47]

Salinity

Salt Overly Sensitive 2; essential for salt-stress signalling and tolerance in Arabidopsis and is known to be activated by calcium-SOS3 and by phosphorylation at its activation loop An SNF1-type serine/threonine protein kinase of wheat (Triticum aestivum L.); confers enhanced multistress tolerance in Arabidopsis, could be utilized in transgenic breeding to improve abiotic stresses in crops Triticum durum dehydrins, belong to DHN gene family, were named on the basis of their identity with known DHN sequences and putative molecular weight Timing of CAB expression 1; a key clock component binds to the promoter of the ABAR and controls its circadian expression Encodes V-H+-PPase from a dicotyledonous halophyte Thellungiella halophila with a maize ubiquitin promoter

[S45]

TaSnRK2.4

Wheat (Triticum aestivum)

Multiple

TdDHN15.2, TdDHN15.1, TdDHN13, TdDHN15.3 and TdDHN9.6 TOC1

Wheat (Triticum durum)

Drought

Arabidopsis

Drought

Dicotyledonous halophyte

Drought

TsVP

Encodes Phospholipase Dα1(one of 12 enzymes that have been identified in Arabidopsis); shown to mediate the ABA regulation of stomatal movements Peroxidase genes Protein phosphatase 2C

[S31] [S2,S8,S10]

[S2,S42]

[S2,S43]

[S2,S40]

[S2,S44]

[S48]

[S16]

[S1] [S49]

4

+

V-H -PPase

V-ATPase WLIP19

(Thellungiella halophila) Dicotyledonous halophyte (Thellungiella halophila) Arabidopsis Wheat (Triticum aestivum)

Drought

Vacuolar H+-pyrophosphatase

[S49]

Elevated temperature Multiple

Vacuolar H+-ATPase

[S32]

Wheat LIP (low-temperature induced protein) 19

[S14]

Supplementary references

S1 Legnaioli, T., et al. (2009) TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J 28, 37453757 S2 Poole, R.L. (2007) The TAIR Database. Methods Mol Biol. 406, 179-212 S3 Oh, S.-J., et al. (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol. 150, 13681379 S4 Perera, I.Y., et al. (2008) Transgenic Arabidopsis plants expressing the type 1 inositol 5-phosphatase exhibit increased drought tolerance and altered abscisic acid signaling. Plant Cell 20, 2876-2893 S5 Sakuma, Y., et al. (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18, 1292-1309 S6 Alexandre, C., et al. (2009) Arabidopsis MSI1 is required for negative regulation of the response to drought stress. Mol Plant 2, 675-687 S7 Mishra, G., et al. (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312, 264-266 S8 Zeller, G., et al. (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. The Plant Journal 58, 1068-1082 S9 Zhu, Y., et al. (2009) Ectopic over-expression of BhHsf1, a heat shock factor from the resurrection plant Boea hygrometrica, leads to increased thermotolerance and retarded growth in transgenic Arabidopsis and tobacco. Plant Molecular Biology 71, 451-467 S10 Zhang, H., et al. (2008) Dolichol biosynthesis and its effects on the unfolded protein response and abiotic stress resistance in Arabidopsis. Plant Cell 20, 1879-1898 S11 Perez, D.E., et al. (2009) BOBBER1 is a noncanonical Arabidopsis small heat shock protein required for both development and thermotolerance. Plant Physiol. 151, 241-252 S12 Liu, H.-T., et al. (2008) The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. The Plant Journal 55, 760-773 S13 Priyanka, B., et al. (2010) Expression of pigeonpea hybrid-proline-rich protein encoding gene (CcHyPRP) in yeast and Arabidopsis affords multiple abiotic stress tolerance. Plant Biotechnology Journal 8, 76-87 S14 Kobayashi, F., et al. (2008) Development of abiotic stress tolerance via bZIP-type transcription factor LIP19 in common wheat. J. Exp. Bot. 59, 891-905 S15 Magome, H., et al. (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. The Plant Journal 56, 613-626 S16 Rampino, P., et al. (2006) Drought stress response in wheat: physiological and molecular analysis of resistant and sensitive genotypes. Plant, Cell and Environment 29, 2143-2152 S17 Qin, F., et al. (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20, 1693-1707 S18 Ning, J., et al. (2010) A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol. 152, 876-890 S19 Springer, C.J., et al. (2008) Elevated CO2 influences the expression of floral-initiation genes in Arabidopsis thaliana. New Phytologist 178, 63-67 S20 Wang, Y., et al. (2009) Shoot-specific down-regulation of protein farnesyltransferase ({alpha}-subunit) for yield protection against drought in Canola. Mol Plant 2, 191-200 S21 Seo, P.J., et al. (2009) The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol. 151, 275-289 S22 Zhou, Q.-Y., et al. (2008) Soybean WRKY-type transcription factor genes,GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnology Journal 6, 486-503 S23 Mishkind, M., et al. (2009) Heat stress activates phospholipase D and triggers PIP2 accumulation at the plasma membrane and nucleus. The Plant Journal 60, 10-21 S24 Kim, J.S., et al. (2008) Glycine-rich RNA-binding protein7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. The Plant Journal 55, 455-466 S25 Lee, U., et al. (2008) Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20, 786-802 S26 Møller, I.S., et al. (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21, 2163-2178

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S27 Quist, T.M., et al. (2009) HOS3, an ELO-like gene, inhibits effects of ABA and implicates a S-1-P/Ceramide control system for abiotic stress responses in Arabidopsis thaliana. Mol Plant 2, 138-151 S28 Schramm, F., et al. (2008) A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. The Plant Journal 53, 264-274 S29 Oh, S.-J., et al. (2007) Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice. Plant Biotechnology Journal 5, 646-656 S30 Fortunati, A., et al. (2008) Isoprene emission is not temperature-dependent during and after severe drought-stress: a physiological and biochemical analysis. The Plant Journal 55, 687-697 S31 Sakamoto, H., et al. (2008) ITN1, a novel gene encoding an ankyrin-repeat protein that affects the ABA-mediated production of reactive oxygen species and is involved in salt-stress tolerance in Arabidopsis thaliana. The Plant Journal 56, 411-422 S32 Barkla, B.J., et al. (2009) Quantitative proteomics of the tonoplast reveals a role for glycolytic enzymes in salt tolerance. Plant Cell 21, 4044-4058 S33 Li, W.-X., et al. (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20, 2238-2251 S34 Ramírez, V., et al. (2009) Drought tolerance in Arabidopsis is controlled by the OCP3 disease resistance regulator. The Plant Journal 58, 578-591 S35 Amir Hossain, M., et al. (2010) The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signaling in rice. Plant Molecular Biology 72, 557-566 S36 Zhang, L., et al. (2009) Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol. 149, 916-928 S37 Rodriguez, A.A., et al. (2009) Polyamine oxidase activity contributes to sustain maize leaf elongation under saline stress. J. Exp. Bot. 60, 4249-4262 S38 Rodriguez-Milla, M.A. and Salinas, J. (2009) Prefoldins 3 and 5 play an essential role in Arabidopsis tolerance to salt stress. Mol Plant 2, 526-534 S39 Hong, Y., et al. (2008) Dual functions of phospholipase D{alpha}1 in plant response to drought. Mol Plant 1, 262-269 S40 Cho, S.K., et al. (2008) Arabidopsis PUB22 and PUB23 are homologous U-Box E3 ubiquitin ligases that play combinatory roles in response to drought stress. Plant Cell 20, 1899-1914 S41 Kurek, I., et al. (2007) Enhanced thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell 19, 3230 - 3241 S42 Lee, H.K., et al. (2009) Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell 21, 622-641 S43 Meiri, D. and Breiman, A. (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. The Plant Journal 59, 387-399 S44 Wilson, P.B., et al. (2009) The nucleotidase/phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis. The Plant Journal 58, 299317 S45 Fujii, H. and Zhu, J.-K. (2009) An autophosphorylation site of the protein kinase SOS2 is important for salt tolerance in Arabidopsis. Mol Plant 2, 183190 S46 Naya, L., et al. (2007) The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to the subsequent recovery of plants. Plant Physiol. 144, 1104-1114 S47 m, Y.J., et al. (2009) Expression of Pyrococcus furiosus superoxide reductase in Arabidopsis enhances heat tolerance. Plant Physiol. 151, 893-904 S48 Mao, X., et al. (2010) TaSnRK2.4, an SNF1-type serine/threonine protein kinase of wheat (Triticum aestivum L.), confers enhanced multistress tolerance in Arabidopsis. J. Exp. Bot. 61, 683-696 S49 Li, B., et al. (2008) Heterologous expression of the TsVPi gene improves the drought resistance of maize. Plant Biotechnology Journal 6, 146-159

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