Group 3 late embryogenesis abundant protein in Arabidopsis: structure, regulation, and function

• Autorzy: Zhao P.S. , Liu F. , Zheng G. C. , Liu H.
• Języki publikacji: EN

Abstrakty

EN

Group 3 late embryogenesis abundant proteins accumulate in maturing seeds, in which their expression correlates with desiccation tolerance. Group 3 proteins are also strongly associated with tolerance for abiotic stresses, such as high salinity, drought, cold, and osmotic stress in vegetative tissues. However, the precise function of these proteins remained obscure for more than 20 years. In this study, the structure of and available regulation information on Group 3 genes/proteins in Arabidopsis are reviewed. The function of Group 3 proteins in response to desiccation and the relationship between protein structure and function are also discussed.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2011
• Tom: 33
• Numer: 4
• Opis fizyczny: p.1063-1073,fig.,ref.

Twórcy

autor

Zhao P.S.

• Institute of Cell Biology, Life Science School, Lanzhou University, Lanzhou 730000, Gansu, Peaple s Republic of China

autor

Liu F.

• Institute of Cell Biology, Life Science School, Lanzhou University, Lanzhou 730000, Gansu, Peaple s Republic of China

autor

Zheng G. C.

• Institute of Cell Biology, Life Science School, Lanzhou University, Lanzhou 730000, Gansu, Peaple s Republic of China

autor

Liu H.

• Institute of Cell Biology, Life Science School, Lanzhou University, Lanzhou 730000, Gansu, Peaple s Republic of China

Bibliografia

• Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78
• Armengaud P, Breitling R, Amtmann A (2004) The potassiumdependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 136:2556–2576
• Babu RC, Zhang J, Blum A, Ho THD, Wu R, Nguyen HT (2004) HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa) via cell membrane protection. Plant Sci 166:855–862
• Bahrndorff S, Tunnacliffe A, Wise MJ, McGee B, Holmstrup M, Loeschcke V (2009) Bioinformatics and protein expression analyses implicate LEA proteins in the drought response of Collembola. J Insect Physiol 55:210–217
• Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA (2008) The enigmatic LEA proteins and other hydrophilins. Plant Physiol 148:6–24
• Battista JR, Park MJ, McLemore AE (2001) Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation. Cryobiology 43:133–139
• Bies-Ethe`ve N, Gaubier-Comella P, Debures A, Lasserre E, Jobet E, Raynal M, Cooke R, Delseny M (2008) Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana. Plant Mol Biol 67:107–124
• Bray EA (1993) Molecular responses to water deficit. Plant Physiol 103:1035–1040
• Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54
• Browne J, Tunnacliffe A, Burnell A (2002) Anhydrobiosis: plant desiccation gene found in a nematode. Nature 416:38
• Bryson K, McGuffin LJ, Marsden RL, Ward JJ, Sodhi JS, Jones DT (2005) Protein structure prediction servers at University College London. Nucl Acids Res 33:W36–W38
• Cao D, Cheng H, Wu W, Soo HM, Peng JR (2006) Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. Plant Physiol 142:509–525
• Caramelo JJ, Iusem ND (2009) When cells lose water: lessons from biophysics and molecular biology. Prog Biophys Mol Biol 99:1–6
• Catala R, Ouyang J, Abreu IA, Hu Y, Seo H, Zhang X, Chua NH (2007) The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses. Plant Cell 19:2952–2966
• Chakrabortee S, Boschetti C, Walton LJ, Sarkar S, Rubinsztein DC, Tunnacliffe A (2007) Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function. Proc Natl Acad Sci USA 104:18073–18078
• Chapman KD (2004) Occurrence, metabolism, and prospective functions of N-acylethanolamines in plants. Prog Lipid Res 43:302–327
• Chapman KD, Venables B, Markovic R, Blair RW Jr, Bettinger C (1999) N-Acylethanolamines in seeds. Quantification of molecular species and their degradation upon imbibition. Plant Physiol 120:1157–1164
• Che P, Gingerich DJ, Lall S, Howell SH (2002) Global and hormoneinduced gene expression changes during shoot development in Arabidopsis. Plant Cell 14:2771–2785
• Cuming AC (1999) LEA proteins. In: Casey R, Shewry PR (eds) Seed proteins. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 753–780
• Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139:847–856
• Dure L (1993a) A repeating 11-mer amino acid motif and plant desiccation. Plant J 3:363–369
• Dure L (1993b) Structural motifs in LEA proteins. In: Close TJ, Bray EA (eds) Plant responses to cellular dehydration during environmental stress. American Society of Plant Physiologists, Rockville, pp 91–103
• Dure L III, Greenway SC, Galau GA (1981) Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis. Biochemistry 20:4162–4168
• Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45
• Fu D, Huang B, Xiao Y, Muthukrishnan S, Liang GH (2007) Overexpression of barley HVA1 gene in creeping bentgrass for improving drought tolerance. Plant Cell Rep 26:467–477
• Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106:8380–8385
• Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M et al (2005) AREB1 is a transcription activator of novel ABREdependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488
• Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N et al (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50:2123–2132
• Gal TZ, Glazer I, Koltai H (2003) Differential gene expression during desiccation stress in the insect-killing nematode Steinernema feltiae IS-6. J Parasitol 89:761–766
• Gal TZ, Glazer I, Koltai H (2004) An LEA group 3 family member is involved in survival of C. elegans during exposure to stress. FEBS Lett 577:21–26
• Gilmour SJ, Artus NN, Thomashow MF (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18:13–21
• Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 134:1555–1573
• Goeres DC, Van Norman JM, Zhang W, Fauver NA, Spencer ML, Sieburth LE (2007) Components of the Arabidopsis mRNA decapping complex are required for early seedling development. Plant Cell 19:1549–1564
• Goyal K, Tisi L, Basran A, Browne J, Burnell A, Zurdo J, Tunnacliffe A (2003) Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. J Biol Chem 278:12977–12984
• Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157
• Grelet J, Benamar A, Teyssier E, Avelange-Macherel MH, Grunwald D, Macherel D (2005) Identification in pea seed mitochondria of a late-embryogenesis abundant protein able to protect enzymes from drying. Plant Physiol 137:157–167
• Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 132:578–596
• Honjoh K-I, Matsumoto H, Shimizu H, Ooyama K, Tanaka K, Oda Y, Takata R, Joh T, Suga K, Miyamoto T, Iio M, Hatano S (2000) Cryoprotective activities of Group 3 late embryogenesis abundant proteins from Chlorella vulgaris C-27. Biosci Biotechnol Biochem 64:1656–1663
• Hou X, Hu WW, Shen L, Lee LY, Tao Z, Han JH, Yu H (2008) Global identification of DELLA target genes during Arabidopsis flower development. Plant Physiol 147:1126–1142
• Hughes DW, Galau GA (1991) Developmental and environmental induction of Lea and LeaA mRNAs and the postabscission program during embryo culture. Plant Cell 3:605–618
• Hundertmark M, Hincha DK (2008) LEA (Late Embryogenesis Abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118–139
• Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403
• Job C, Rajjou L, Lovigny Y, Belghazi M, Job D (2005) Patterns of protein oxidation in Arabidopsis seeds and during germination. Plant Physiol 138:790–802
• Kaplan B, Davydov O, Knight H, Galon Y, Knight MR, Fluhr R, Fromm H (2006) Rapid transcriptome changes induced by cytosolic Ca²⁺ transients reveal ABRE-related sequences as Ca²⁺-responsive cis elements in Arabidopsis. Plant Cell 18:2733–2748
• Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141
• Kurkela S, Borg-Franck M (1992) Structure and expression of kin2, one of two cold- and ABA-induced genes of Arabidopsis thaliana. Plant Mol Biol 19(4):689–692
• Kurkela S, Franck M (1990) Cloning and characterization of a coldand ABA-inducible Arabidopsis gene. Plant Mol Biol 15(1):137–144
• Lal S, Gulyani V, Khurana P (2008) Overexpression of HVA1 gene from barley generates tolerance to salinity and water stress in transgenic mulberry (Morus indica). Transgenic Res 17:651–663
• Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis coldresponsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175
• Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI (2005) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16:596–615
• Li Y, Lee KK, Walsh S, Smith C, Hadingham S, Sorefan K, Cawley G, Bevan MW (2006) Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using relevance vector machine. Genome Res 16:414–427
• Liu Y, Zheng Y (2005) PM2, a group 3 LEA protein from soybean, and its 22-mer repeating region confer salt tolerance in Escherichia coli. Biochem Biophys Res Commun 331:325–332
• Liu XJ, Srivastava R, Che P, Howell ST (2007) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51:897–909
• Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A et al (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068
• Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H et al (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38:982–993
• Melcher K, Ng LM, Zhou XE, Soon FF, Xu Y, Suino-Powell KM et al (2009) A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 462:602–608
• Menze MA, Boswell L, Toner M, Hand SC (2009) Occurrence of mitochondria-targeted late embryogenesis abundant (LEA) gene in animals increases organelle resistance to water stress. J Biol Chem 284:10714–10719
• Miura K, Lee J, Jina JB, Yooa CY, Miura T, Hasegawa PM (2009) Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc Natl Acad Sci USA 106:5418–5423
• Mizoguchi M, Umezawa T, Nakashima K, Kidokoro S, Takasaki H, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2010) Two closely related subclass II SnRK2 protein kinases cooperatively regulate drought-inducible gene expression. Plant Cell Physiol 51(5):842–847
• Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41:697–709
• Nakamura S, Lynch T, Finkelstein R (2001) Physical interactions between ABA response loci of Arabidopsis. Plant J 26:627–635
• Nakashima K, FujitaY, KanamoriN, Katagiri T,Umezawa T,Kidokoro S et al (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/ SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50:1345–1363
• Nakayama K, Okawa K, Kakizaki T, Honma T, Itoh H, Inaba T (2007) Arabidopsis Cor15am is a chloroplast stromal protein that has cryoprotective activity and forms oligomers. Plant Physiol 144:513–523
• O’Connor TR, Dyreson C, Wyrick JJ (2005) Athena: a resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences. Bioinformatics 21:4411–4413
• Oliver M, Dowd S, Zaragoza J, Mauget S, Payton P (2004) The rehydration transcriptome of the desiccation-tolerant bryophyte Tortula ruralis: transcript classification and analysis. BMC Genomics 5:89
• Park B-J, Liu ZC, Kanno A, Kameya T (2005) Genetic improvement of Chinese cabbage for salt and drought tolerance by constitutive expression of a B. napus LEA gene. Plant Sci 169:553–558
• Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071
• Pouchkina-Stantcheva NN, McGee BM, Boschetti C, Tolleter D, Chakrabortee S, Popova AV et al (2007) Functional divergence of former alleles in an ancient asexual invertebrate. Science 318:268–271
• Rajjou L, Belghazi M, Huguet R, Robin C, Moreau A, Job C, Job D (2006) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141:910–923
• Rashotte AM, Carson SDB, To JPC, Kieber JJ (2003) Expression profiling of cytokinin action in Arabidopsis. Plant Physiol 132:1998–2011
• Reyes JL, Rodrigo MJ, Colmenero-Flores JM, Gil JV, Garay-Arroyo A et al (2005) Hydrophilins from distant organisms can protect enzymatic activities from water limitation effects in vitro. Plant Cell Environ 28:709–718
• Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696
• Rohila JS, Jain RK, Wu R (2002) Genetic improvement of Basmati rice for salt and drought tolerance by regulated expression of a barley Hva1 cDNA. Plant Sci 163:525–532
• Saez A, Robert N, Maktabi MH, Schroeder JI, Serrano R, Rodriguez PL (2006) Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB1. Plant Physiol 141:1389–1399
• Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309
• Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006b) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822–18827
• Shih M, Lin S, Hsieh J, Tsou C, Chow T, Lin T, Hsing Y (2004) Gene cloning and characterization of a soybean (Glycine max L.) LEA protein, GmPM16. Plant Mol Biol 56:689–703
• Shih M-D, Hoekstra FA, Hsing Y-I (2008) Late embryogenesis abundant proteins. Adv Bot Res 48:212–255
• Sivamani E, Bahieldin A, Wraith JM, Al-Niemi T, Dyer WE, Ho TD, Qu R (2000) Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. Plant Sci 155:1–9
• Soitamo AJ, Piippo M, Allahverdiyeva Y, Battchikova N, Aro EM (2008) Light has a specific role in modulating Arabidopsis gene expression at low temperature. BMC Plant Biol 8:13
• Suzuki M, Ketterling MG, Li QB, McCarty DR (2003) Viviparous1 alters global gene expression patterns through regulation of abscisic acid signaling. Plant Physiol 132:1664–1677
• Tai HH, Tai GC, Beardmore T (2005) Dynamic histone acetylation of late embryonic genes during seed germination. Plant Mol Biol 59:909–925
• Teaster ND, Motes CM, Tang Y, Wiant WC, Cotter MQ, Wang YS et al (2007) N-Acylethanolamine metabolism interacts with abscisic acid signaling in Arabidopsis thaliana seedlings. Plant Cell 19:2454–2469
• Thalhammer A, Hundertmark M, Popova AV, Seckler R, Hincha DK (2010) Interaction of two intrinsically disordered plant stress proteins (COR15A and COR15B) with lipid membranes in the dry state. Biochim Biophys Acta 1798:1812–1820
• Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599
• Tolleter D, Jaquinod M, Mangavel C, Passirani C, Saulnier P, Manon S et al (2007) Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation. Plant Cell 19:1580–1589
• Tolleter D, Hincha DK, Macherel D (2010) A mitochondrial late embryogenesis abundant protein stabilizes model membranes in the dry state, Biochim Biophys Acta. doi:10.1016/j.bbamem. 2010.06.029
• Tunnacliffe A, Wise MJ (2007) The continuing conundrum of LEA proteins. Naturwissenschaften 94:791–812
• Wang L, Li X, Chen S, Liu G (2009) Enhanced drought tolerance in transgenic Leymus chinensis plants with constitutively expressed wheat TaLEA3. Biotechnol Lett 31:313–319
• Wise MJ (2003) LEAping to conclusions: a computational reanalysis of late embryogenesis abundant proteins and their possible roles. BMC Bioinform 4:52
• Wise MJ, Tunnacliffe A (2004) POPP the question: what do LEA proteins do? Trends Plant Sci 9:13–17
• Wolkers WF, McCready S, Brandt WF, Lindsey GG, Hoekstra FA (2001) Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro. Biochim Biophys Acta 1544:196–206
• Xu D, Duan X, Wang B, Hong B, Ho T, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249–257
• Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803
• Yu JN, Zhang JS, Shan L, Chen SY (2005) Two new group 3 LEA genes of wheat and their functional analysis in yeast. J Integr Plant Biol 47:1372–1381
• Zhang L, Ohta A, Takagi M, Imai R (2000) Expression of plant Group 2 and Group 3 lea genes in Saccharomyces cerevisiae revealed functional divergence among LEA proteins. J Biochem 127:611–616
• Zhang Y, Cao G, Qu LJ, Gu H (2009) Involvement of an R2R3-MYB transcription factor gene AtMYB118 in embryogenesis in Arabidopsis. Plant Cell Rep 28:337–346
• Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
• Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC et al (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036

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