Skip to main content
SpringerLink
Log in

Twenty years of research on Asr (ABA-stress-ripening) genes and proteins

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Investigating how plants cope with different abiotic stresses—mainly drought and extreme temperatures—is pivotal for both understanding the underlying signaling pathways and improving genetically engineered crops. Plant cells are known to react defensively to mild and severe dehydration by initiating several signal transduction pathways that result in the accumulation of different proteins, sugar molecules and lipophilic anti-oxidants. Among the proteins that build up under these adverse conditions are members of the ancestral ASR (ABA-stress-ripening) family, which is conserved in the plant kingdom but lacks orthologs in Arabidopsis. This review provides a comprehensive summary of the state of the art regarding ASRs, going back to the original description and cloning of the tomato ASR cDNA. That seminal discovery sparked worldwide interest amongst research groups spanning multiple fields: biochemistry, cell biology, evolution, physiology and epigenetics. As these proteins function as both chaperones and transcription factors; this review also covers the progress made on relevant molecular features that account for these dual roles—including the recent identification of their target genes—which may inspire future basic research. In addition, we address reports of drought-tolerant ASR-transgenic plants of different species, highlighting the influential work of authors taking more biotechnological approaches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Amitai-Zeigerson H, Scolnik PA, Bar-Zvi D (1995) Tomato Asr1 mRNA and protein are transiently expressed following salt stress, osmotic stress and treatment with abscisic acid. Plant Sci 110:205–213

    Article  CAS  Google Scholar 

  • Arenhart RA, Margis R, Margis-Pinheiro M (2012) The rice ASR5 protein: a putative role in the response to aluminium photosynthesis disturbance. Plant Signal Behav 7:1263–1266

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Arenhart RA, Bai Y, Valter de Oliveira LF, Bucker Neto L, Schunemann M, Maraschin FD, Mariath J, Silverio A, Sachetto-Martins G, Margis R, Wang ZY, Margis-Pinheiro M (2013a) New Insights into Aluminum Tolerance in Rice: The ASR5 Protein Binds the STAR1 Promoter and Other Aluminum-Responsive Genes. Mol Plant [Epub ahead of print]

  • Arenhart RA, Lima JC, Pedron M, Carvalho FE, Silveira JA, Rosa SB, Caverzan A, Andrade CM, Schunemann M, Margis R, Margis-Pinheiro M (2013b) Involvement of ASR genes in aluminium tolerance mechanisms in rice. Plant Cell Environ 36:52–67

    Article  PubMed  CAS  Google Scholar 

  • Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA (2008) The enigmatic LEA proteins and other hydrophilins. Plant Physiol 148:6–24

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bazargani MM, Sarhadi E, Bushehri AA, Matros A, Mock HP, Naghavi MR, Hajihoseini V, Mardi M, Hajirezaei MR, Moradi F, Ehdaie B, Salekdeh GH (2011) A proteomics view on the role of drought-induced senescence and oxidative stress defense in enhanced stem reserves remobilization in wheat. J Proteomics 74:1959–1973

    Article  PubMed  CAS  Google Scholar 

  • Bermudez-Moretti M, Maskin L, Gudesblat G, García SC, Iusem ND (2006) ASR1, a stress-induced tomato protein, protects yeast from osmotic stress. Physiol Plant 127:111–118

    Article  CAS  Google Scholar 

  • Cakir B, Agasse A, Gaillard C, Saumonneau A, Delrot S, Atanassova R (2003) A grape ASR protein involved in sugar and abscisic acid signaling. Plant Cell 15:2165–2180

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Caramelo JJ, Iusem ND (2009) When cells lose water: lessons from biophysics and molecular biology. Prog Biophys Mol Biol 99:1–6

    Article  PubMed  CAS  Google Scholar 

  • Carrari F, Fernie AR, Iusem ND (2004) Heard it through the grapevine? ABA and sugar cross-talk: the ASR story. Trends Plant Sci 9:57–59

    Article  PubMed  CAS  Google Scholar 

  • Cortes AJ, Chavarro MC, Madrinan S, This D, Blair MW (2012) Molecular ecology and selection in the drought-related Asr gene polymorphisms in wild and cultivated common bean (Phaseolus vulgaris L.). BMC Genet 13:58

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dai JR, Liu B, Feng DR, Liu HY, He YM, Qi KB, Wang HB, Wang JF (2011) MpAsr encodes an intrinsically unstructured protein and enhances osmotic tolerance in transgenic Arabidopsis. Plant Cell Rep 30:1219–1230

    Article  PubMed  CAS  Google Scholar 

  • Dóczi R, Csanaki C, Bánfalvi Z (2002) Expression and promoter activity of the desiccation-specific Solanum tuberosum gene, StDS2. Plant Cell Environ 25:1197–1203

    Article  Google Scholar 

  • Dominguez PG, Frankel N, Mazuch J, Balbo I, Iusem N, Fernie AR, Carrari F (2013) ASR1 mediates glucose-hormone cross talk by affecting sugar trafficking in tobacco plants. Plant Physiol 161:1486–1500

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fischer I, Camus-Kulandaivelu L, Allal F, Stephan W (2011) Adaptation to drought in two wild tomato species: the evolution of the Asr gene family. New Phytol 190:1032–1044

    Article  PubMed  Google Scholar 

  • Fischer I, Steige KA, Stephan W, Mboup M (2013) Sequence evolution and expression regulation of stress-responsive genes in natural populations of wild tomato. PLoS ONE 8:e78182

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Frankel N, Hasson E, Iusem ND, Rossi MS (2003) Adaptive evolution of the water stress-induced gene Asr2 in Lycopersicon species dwelling in arid habitats. Mol Biol Evol 20:1955–1962

    Article  PubMed  CAS  Google Scholar 

  • Frankel N, Carrari F, Hasson E, Iusem ND (2006) Evolutionary history of the Asr gene family. Gene 378:74–83

    Article  PubMed  CAS  Google Scholar 

  • Frankel N, Nunes-Nesi A, Balbo I, Mazuch J, Centeno D, Iusem ND, Fernie AR, Carrari F (2007) ci21A/Asr1 expression influences glucose accumulation in potato tubers. Plant Mol Biol 63:719–730

    Article  PubMed  CAS  Google Scholar 

  • Giombini MI, Frankel N, Iusem ND, Hasson E (2009) Nucleotide polymorphism in the drought responsive gene Asr2 in wild populations of tomato. Genetica 136:13–25

    Article  PubMed  CAS  Google Scholar 

  • Goldgur Y, Rom S, Ghirlando R, Shkolnik D, Shadrin N, Konrad Z, Bar-Zvi D (2007) Desiccation and zinc binding induce transition of tomato abscisic acid stress ripening 1, a water stress- and salt stress-regulated plant-specific protein, from unfolded to folded state. Plant Physiol 143:617–628

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gonzalez RM, Ricardi MM, Iusem ND (2011) Atypical epigenetic mark in an atypical location: cytosine methylation at asymmetric (CNN) sites within the body of a non-repetitive tomato gene. BMC Plant Biol 11:94

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gonzalez RM, Ricardi MM, Iusem ND (2013) Epigenetic marks in an adaptive water stress-responsive gene in tomato roots under normal and drought conditions. Epigenetics 8(8):864–872

    Google Scholar 

  • Henry IM, Carpentier SC, Pampurova S, Van Hoylandt A, Panis B, Swennen R, Remy S (2011) Structure and regulation of the Asr gene family in banana. Planta 234:785–798

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hsu YF, Yu SC, Yang CY, Wang CS (2011) Lily ASR protein-conferred cold and freezing resistance in Arabidopsis. Plant Physiol Biochem 49:937–945

    Article  PubMed  CAS  Google Scholar 

  • Hu W, Huang C, Deng X, Zhou S, Chen L, Li Y, Wang C, Ma Z, Yuan Q, Wang Y, Cai R, Liang X, Yang G, He G (2013) TaASR1, a transcription factor gene in wheat, confers drought stress tolerance in transgenic tobacco. Plant Cell Environ 36:1449–1464

    Article  PubMed  CAS  Google Scholar 

  • Huang JC, Lin SM, Wang CS (2000) A pollen-specific and desiccation-associated transcript in Lilium longiflorum during development and stress. Plant Cell Physiol 41:477–485

    Article  PubMed  CAS  Google Scholar 

  • Hunault G, Jaspard E (2010) LEAPdb: a database for the late embryogenesis abundant proteins. BMC Genom 11:221

    Article  CAS  Google Scholar 

  • Iusem ND, Bartholomew DM, Hitz WD, Scolnik PA (1993) Tomato (Lycopersicon esculentum) transcript induced by water deficit and ripening. Plant Physiol 102:1353–1354

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jaspard E, Macherel D, Hunault G (2012) Computational and statistical analyses of amino acid usage and physico-chemical properties of the twelve late embryogenesis abundant protein classes. PLoS ONE 7(5):e36968

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jeanneau M, Gerentes D, Foueillassar X, Zivy M, Vidal J, Toppan A, Perez P (2002) Improvement of drought tolerance in maize: towards the functional validation of the Zm-Asr1 gene and increase of water use efficiency by over-expressing C4-PEPC. Biochimie 84:1127–1135

    Article  PubMed  CAS  Google Scholar 

  • Jha B, Agarwal PK, Reddy PS, Lal S, Sopory SK, Reddy MK (2009) Identification of salt-induced genes from Salicornia brachiata, an extreme halophyte through expressed sequence tags analysis. Genes Genet Syst 84:111–120

    Article  PubMed  CAS  Google Scholar 

  • Jha B, Lal S, Tiwari V, Yadav SK, Agarwal PK (2012) The SbASR-1 gene cloned from an extreme halophyte Salicornia brachiata enhances salt tolerance in transgenic tobacco. Mar Biotechnol (NY) 14:782–792

    Article  CAS  Google Scholar 

  • Joo J, Lee Y, Choi D, Cheong J-J, Kim Y-K, Song S (2013a) Rice ASR1 has function in abiotic stress tolerance during early growth stages of rice. J Korean Soc Appl Biol Chem 56:349–352

    Article  CAS  Google Scholar 

  • Joo J, Lee Y, Kim Y-K, Nahm B, Song S (2013b) Abiotic stress responsive rice ASR1 and ASR3 exhibit different tissue-dependent sugar and hormone-sensitivities. Mol Cells 35:421–435

    Article  PubMed  CAS  Google Scholar 

  • Kalifa Y, Gilad A, Konrad Z, Zaccai M, Scolnik PA, Bar-Zvi D (2004a) The water- and salt-stress-regulated Asr1 (abscisic acid stress ripening) gene encodes a zinc-dependent DNA-binding protein. Biochem J 381:373–378

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kalifa Y, Perlson E, Gilad A, Konrad Z, Scolnik PA, Bar-Zvi D (2004b) Over-expression of the water and salt stress-regulated Asr1 gene confers an increased salt tolerance. Plant Cell Environ 27:1459–1468

    Article  CAS  Google Scholar 

  • Kim SJ, Lee SC, Hong SK, An K, An G, Kim SR (2009) Ectopic expression of a cold-responsive OsAsr1 cDNA gives enhanced cold tolerance in transgenic rice plants. Mol Cells 27:449–458

    Article  PubMed  CAS  Google Scholar 

  • Konrad Z, Bar-Zvi D (2008) Synergism between the chaperone-like activity of the stress regulated ASR1 protein and the osmolyte glycine-betaine. Planta 227:1213–1219

    Article  PubMed  CAS  Google Scholar 

  • Li RH, Liu GB, Wang H, Zheng YZ (2013) Effects of Fe3+ and Zn2+ on the structural and thermodynamic properties of a soybean ASR protein. Biosci Biotechnol Biochem 77:475–481

    PubMed  CAS  Google Scholar 

  • Maskin L, Gudesblat GE, Moreno JE, Carrari FO, Ns Frankel, An Sambade, Rossi M, Iusem ND (2001) Differential expression of the members of the Asr gene family in tomato (Lycopersicon esculentum). Plant Sci 161:739–746

    Article  CAS  Google Scholar 

  • Maskin L, Frankel N, Gudesblat G, Demergasso MJ, Pietrasanta LI, Iusem ND (2007) Dimerization and DNA-binding of ASR1, a small hydrophilic protein abundant in plant tissues suffering from water loss. Biochem Biophys Res Commun 352:831–835

    Article  PubMed  CAS  Google Scholar 

  • Maskin L, Maldonado S, Iusem ND (2008) Tomato leaf spatial expression of stress-induced Asr genes. Mol Biol Rep 35:501–505

    Article  PubMed  CAS  Google Scholar 

  • Padmanabhan V, Dias DM, Newton RJ (1997) Expression analysis of a gene family in loblolly pine (Pinus taeda L.) induced by water deficit stress. Plant Mol Biol 35:801–807

    Article  PubMed  CAS  Google Scholar 

  • Perez-Diaz J, Wu TM, Perez-Diaz R, Ruiz-Lara S, Hong CY, Casaretto JA (2014) Organ- and stress-specific expression of the ASR genes in rice. Plant Cell Rep 33(1):61–73

    Google Scholar 

  • Philippe R, Courtois B, McNally KL, Mournet P, El-Malki R, Le Paslier MC, Fabre D, Billot C, Brunel D, Glaszmann JC, This D (2010) Structure, allelic diversity and selection of Asr genes, candidate for drought tolerance, in Oryza sativa L. and wild relatives. Theor Appl Genet 121:769–787

    Article  PubMed  CAS  Google Scholar 

  • Ricardi MM, Guaimas FF, Gonzalez RM, Burrieza HP, Lopez-Fernandez MP, Jares-Erijman EA, Estevez JM, Iusem ND (2012) Nuclear import and dimerization of tomato ASR1, a water stress-inducible protein exclusive to plants. PLoS ONE 7:e41008

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ricardi MM, González RM, Zhong S, Domínguez PG, Duffy T, Turjanski PG, Salgado Salter JD, Alleva K, Carrari F, Giovannoni JJ, Estévez JM, Iusem ND (2014) Genome-wide data (ChIP-seq) enabled identification of cell wall-related and aquaporin genes as targets of tomato ASR1, a drought stress-responsive transcription factor. BMC Plant Biol 14(1):29

    Article  PubMed Central  PubMed  Google Scholar 

  • Rom S, Gilad A, Kalifa Y, Konrad Z, Karpasas MM, Goldgur Y, Bar-Zvi D (2006) Mapping the DNA- and zinc-binding domains of ASR1 (abscisic acid stress ripening), an abiotic-stress regulated plant specific protein. Biochimie 88:621–628

    Article  PubMed  CAS  Google Scholar 

  • Rossi M, Iusem ND (1994) Tomato (Lycopersicon esculentum) genomic clone homologous to a gene encoding an abscisic acid-induced protein. Plant Physiol 104:1073–1074

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rossi M, Iusem ND (1995) Sequence of Asr2, a member of a gene family from Lycopersicon esculentum encoding chromosomal proteins: homology to an intron of the polygalacturonase gene. DNA Seq 5:225–227

    PubMed  CAS  Google Scholar 

  • Rossi M, Lijavetzky D, Bernacchi D, Hopp HE, Iusem N (1996) Asr genes belong to a gene family comprising at least three closely linked loci on chromosome 4 in tomato. Mol Gen Genet 252:489–492

    PubMed  CAS  Google Scholar 

  • Rossi M, Carrari F, Cabrera-Ponce JL, Vazquez-Rovere C, Herrera-Estrella L, Gudesblat G, Iusem ND (1998) Analysis of an abscisic acid (ABA)-responsive gene promoter belonging to the Asr gene family from tomato in homologous and heterologous systems. Mol Gen Genet 258:1–8

    Article  PubMed  CAS  Google Scholar 

  • Saumonneau A, Agasse A, Bidoyen MT, Lallemand M, Cantereau A, Medici A, Laloi M, Atanassova R (2008) Interaction of grape ASR proteins with a DREB transcription factor in the nucleus. FEBS Lett 582:3281–3287

    Article  PubMed  CAS  Google Scholar 

  • Shkolnik D, Bar-Zvi D (2008) Tomato ASR1 abrogates the response to abscisic acid and glucose in Arabidopsis by competing with ABI4 for DNA binding. Plant Biotechnol J 6:368–378

    Article  PubMed  CAS  Google Scholar 

  • Silhavy D, Hutvagner G, Barta E, Banfalvi Z (1995) Isolation and characterization of a water-stress-inducible cDNA clone from Solanum chacoense. Plant Mol Biol 27:587–595

    Article  PubMed  CAS  Google Scholar 

  • Takasaki H, Mahmood T, Matsuoka M, Matsumoto H, Komatsu S (2008) Identification and characterization of a gibberellin-regulated protein, which is ASR5, in the basal region of rice leaf sheaths. Mol Genet Genomics 279:359–370

    Article  PubMed  CAS  Google Scholar 

  • Urtasun N, Correa Garcia S, Iusem ND, Bermudez Moretti M (2010) Predominantly cytoplasmic localization in yeast of ASR1, a non-receptor transcription factor from plants. Open Biochem J 4:68–71

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Virlouvet L, Jacquemot MP, Gerentes D, Corti H, Bouton S, Gilard F, Valot B, Trouverie J, Tcherkez G, Falque M, Damerval C, Rogowsky P, Perez P, Noctor G, Zivy M, Coursol S (2011) The ZmASR1 protein influences branched-chain amino acid biosynthesis and maintains kernel yield in maize under water-limited conditions. Plant Physiol 157:917–936

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wang C-S, Wu T-D, Chung C-KW, Lord EM (1996) Two classes of pollen-specific, heat-stable proteins in Lilium longiflorum. Physiol Plant 97:643–650

    Article  CAS  Google Scholar 

  • Wang J-T, Gould J, Padmanabhan V, Newton R (2002) Analysis and localization of the water-deficit stress-induced gene (lp3). J Plant Growth Regul 21:469–478

    Article  CAS  Google Scholar 

  • Wang H-J, Hsu C-M, Jauh GY, Wang C-S (2005) A lily pollen ASR protein localizes to both cytoplasm and nuclei requiring a nuclear localization signal. Physiol Plant 123:314–320

    Article  CAS  Google Scholar 

  • Wang CS, Hsu SW, Hsu YF (2013) New insights into desiccation-associated gene regulation by Lilium longiflorum ASR during pollen maturation and in transgenic Arabidopsis. Int Rev Cell Mol Biol 301:37–94

    Article  PubMed  CAS  Google Scholar 

  • Yang CY, Chen YC, Jauh GY, Wang CS (2005) A Lily ASR protein involves abscisic acid signaling and confers drought and salt resistance in Arabidopsis. Plant Physiol 139:836–846

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yang CY, Wu CH, Jauh GY, Huang JC, Lin CC, Wang CS (2008) The LLA23 protein translocates into nuclei shortly before desiccation in developing pollen grains and regulates gene expression in Arabidopsis. Protoplasma 233:241–254

    Article  PubMed  CAS  Google Scholar 

  • Yang SH, Kim SH, Berberich T, Kusano T (2012) Identification and properties of a small protein that interacts with a tobacco bZIP-type transcription factor TBZF. Plant Biotechnol 29:395–399

    Article  Google Scholar 

Download references

Acknowledgments

The authors are indebted to the following Argentinian institutions: CONICET (Consejo Nacional de Investigaciones Científicas y Tecnológicas) for salaries, fellowships and grants, ANPCyT (Agencia Nacional de Promoción de Ciencia y Tecnología) for grants and UBA (the University of Buenos Aires) for salaries and grants. The authors are also thankful to the Editor and the anonymous reviewers for constructive comments and suggestions.

Author information

Authors and Affiliations

  1. Instituto de Fisiología, Biología Molecular y Neurociencias (IFIByNE)-CONICET, Buenos Aires, Argentina

    Rodrigo M. González & Norberto D. Iusem

  2. Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina

    Norberto D. Iusem

Authors
  1. Rodrigo M. González
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Norberto D. Iusem
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Norberto D. Iusem.

Rights and permissions

Reprints and permissions

About this article

Cite this article

González, R.M., Iusem, N.D. Twenty years of research on Asr (ABA-stress-ripening) genes and proteins. Planta 239, 941–949 (2014). https://doi.org/10.1007/s00425-014-2039-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-014-2039-9

Keywords

Search

Navigation