Skip to main content

Advertisement

SpringerLink
Log in

Structural evolution and function of stress associated proteins in regulating biotic and abiotic stress responses in plants

  • Review Article
  • Published:
Journal of Plant Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Adverse environmental conditions greatly influence crop production every year and threaten food security. Plants have a range of signaling networks to combat these stresses, in which several stress-responsive genes and regulatory proteins function together. One such important family of proteins, the Stress Associated Protein (SAP) family, has been identified as a novel regulator of multiple stresses. The SAPs possess a characteristic N-terminal A20 zinc-finger domain combined with either AN1 or C2H2 at the C-terminus. SAPs provide tolerance against various abiotic stresses, including cold, salt, drought, heavy metal, and wounding. The majority of SAPs are stress-inducible and have a function in conferring stress tolerance in transgenics. The role of SAPs in regulating biotic stress responses is a newly emerging field among researchers. SAPs interact with many other proteins to execute their functions; however, the detailed mechanism of these interactions needs to be elucidated. In this context, the present review provides a detailed view of the evolution and functions of SAPs in plants. The involvement in crosstalk between abiotic and biotic stress signaling pathways makes SAPs ideal targets to develop crops with tolerance against multiple stresses without any yield penalty. Altogether, we provide current knowledge on SAPs for investigating their role in stress response, which can further be exploited to develop climate-resilient crops through transgene-based, breeding-mediated, or genome-editing 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
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

ACC:

1-Aminocyclopropane-carboxylic acid

ATAF:

Arabidopsis Transcription Activation Factor

bZIP:

Basic Leucine Zipper

CAT:

Catalase

CCH:

Copper Transport Proteins

CK:

Cytokinin

CO1:

Constant1

DI19-4:

Drought-Induced gene family

DREB:

Dehydration Responsive Element Binding protein

DRIP:

DREB2A Interacting Protein

ENO-1:

Enolase 1

ET:

Ethylene

FT:

Flowering locus T

GA:

Gibberellic Acid

GPX-8:

Glutathione Peroxidase 8

GRF-1:

Growth Regulating Factor-1

GSTUs:

Glutathione S Transferase

JA:

Jasmonic Acid

LEA:

Late Embryogenesis Abundant Protein

LOS-2:

Low expression of Osmotically Responsive Gene-2

LSE:

Lineage Specific Expansion

MAPK:

Mitogen Activate Protein Kinase

NADP:

Nicotinamide adenine dinucleotide phosphate

NADP-ME:

NADP Malic Enzyme

NAM:

No Apical Meristem

NCED:

9-cis-Epoxycarotenoid dioxygenase gene

NEMO:

NF-kappa B Essential Modulator

NMR:

Nuclear Magnetic Resource Imaging

NPR1:

Nonexpresser of PR1 gene

OTU:

Ovarian Tumour

PEG:

Polyethylene Glycol

POD:

Peroxidase

PUB1:

Plant U-box Protein 1

RAD23:

Radiation sensitive 23

RAS1:

Response to ABA and Salt 1

RIP1:

Receptor Interacting serine/threonine Kinase Protein1

RLCK253:

Receptor Like Cytoplasmic Kinase 253

ROS:

Reactive Oxygen Species

SA:

Salicylic Acid

SAPs:

Stress Associated Proteins

SOC1:

Suppressor of Overexpression of CO1

SOD:

Superoxide Dismutase

TIP:

Tonoplast Intrinsic Protein

TOR:

Target of Rapamycin

UBA:

Ubiquitin Associated Domain

UIM:

Ubiquitin Interacting Motif

VIGS:

Virus Induced Gene Silencing

WRKYs:

Transcription factor associated with drought stress

ZFPs:

Zinc Finger Proteins

References

  • Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868

    CAS  PubMed  PubMed Central  Google Scholar 

  • Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

    CAS  PubMed  Google Scholar 

  • Agarwal PK, Jha B (2010) Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol Plant 54:201–212

    CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    CAS  Google Scholar 

  • Atkinson NJ, Lilley CJ, Urwin PE (2013) Identification of genes involved in the response to simultaneous biotic and abiotic stress. Plant Physiol 162:2028–2041

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baidyussen A, Aldammas M, Kurishbayev A, Myrzabaeva M, Zhubatkanov A, Sereda G, Porkhun R, Sereda S, Jatayev S, Langridge P, Schramm C, Jenkins LD, Soole KL, Shavrukov Y (2020) Identification, gene expression and genetic polymorphism of zinc finger A20/AN1 stress-associated genes, HvSAP, in salt stressed barley from Kazakhstan. BMC Plant Biol 20:156

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 21:1–36

    Google Scholar 

  • Ben SR, Fabre D, Mieulet D, Meynard D, Dingkuhn M, Al-Doss A, Guiderdoni E, Hassairi A (2012) Expression of the Aeluropus littoralis AlSAP gene in rice confers broad tolerance to abiotic stresses through maintenance of photosynthesis. Plant Cell Environ 35:626–643

    Google Scholar 

  • Ben SR, Romdhane BW, Mihoubi W, Hsouna BA, Brini F (2020) A Lobularia maritima LmSAP protein modulates gibberellic acid homeostasis via its A20 domain under abiotic stress conditions. PLoS One 15:e0233420

    Google Scholar 

  • Bubici C, Papa S, Dean K, Franzoso G (2006) Mutual cross-talk between reactive oxygen species and nuclear factor-kappa B: molecular basis and biological significance. Oncogene 25:6731–6748

    CAS  PubMed  Google Scholar 

  • Busk PK, Page M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–435

    CAS  PubMed  Google Scholar 

  • Chang L, Chang HH, Chang JC, Lu HC, Wang TT, Hsu DW, Tzean Y, Cheng AP, Chiu SY, Yeh HH (2018) Plant A20/AN1 protein serves as the important hub to mediate antiviral immunity. PloS Pathogens 14:e1007288

    PubMed  PubMed Central  Google Scholar 

  • Charrier A, Lelièvre E, Limami AM, Planchet E (2013) Medicago truncatula stress associated protein 1 gene (MtSAP1) overexpression confers tolerance to abiotic stress and impacts proline accumulation in transgenic tobacco. J Plant Physiol 170:874–877

    CAS  PubMed  Google Scholar 

  • Choi H, Han S, Shin D, Lee S (2012) Polyubiquitin recognition by AtSAP5, an A20-type zinc finger containing protein from Arabidopsis thaliana. Biochem Biophys Res Commun 419:436–440

    CAS  PubMed  Google Scholar 

  • Christine GG, Marie LG, Elisabeth P, Pascale S, Anis ML, Eric L (2011) A stress-associated protein containing A20/AN1 zing-finger domains expressed in Medicago truncatula seeds. Plant Physiol Biochem 49:303–310

    Google Scholar 

  • Cushman JC, Bohnert HJ (2000) Genome approaches to plant stress tolerance. Current Opinion in Plant Biology; 3: 117–124. Emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Google Scholar 

  • Dixit A, Tomar P, Vaine E, Abdullah H, Hazen S, Dhankher OP (2018) A stress-associated protein AtSAP13, from Arabidopsis thaliana provides tolerance to multiple abiotic stresses. Plant Cell Environ 41:1171–1185

    CAS  PubMed  Google Scholar 

  • Dixit AR, Dhankher OP (2011) A novel stress-associated protein “AtSAP10” from Arabidopsis thaliana confers tolerance to nickel, manganese, zinc, and high temperature stress. PLoS ONE 6:e20921

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong Q, Duan D, Zhao S, Xu B, Luo J, Wang Q, Huang D, Liu C, Li C, Gong X, Mao K, Ma F (2018) Genome-wide analysis and cloning of the apple stress-associated protein gene family reveals MdSAP15, which confers tolerance to drought and osmotic stresses in transgenic arabidopsis. Int J Mol Sci 19:2478

    PubMed Central  Google Scholar 

  • Duan W, Sun B, Li TW, Tan BJ, Lee MK, Teo TS (2000) Cloning and characterization of AWP1, a novel protein that associates with serine/threonine kinase PRK1 in vivo. Gene 256:113–121

    CAS  PubMed  Google Scholar 

  • Feehan JM, Castel B, Bentham AR, Jones JD (2020) Plant NLRs get by with a little help from their friends. Curr Opin Plant Biol 56:99–108

    CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2016) Stress-triggered redox signaling: what’s in prospect. Plant Cell Environ 39:951–964

    CAS  PubMed  Google Scholar 

  • Gao W, Lu L, Xinquan T, Jinjing J, Huili L, Hui Z, Fuchun X, Chunpeng S (2016) Genome-wide identification and expression analysis of stress-associated proteins (SAPs) containing A20/AN1 zinc finger in cotton. Mol Genet Genom 291:2199–2213

    CAS  Google Scholar 

  • Giri J, Dansana PK, Kothari KS, Sharma G, Vij S, Tyagi AK (2013) SAPs as novel regulators of abiotic stress response in plants. BioEssays 35:639–648

    CAS  PubMed  Google Scholar 

  • Giri J, Vij S, Dansana PK, Tyagi AK (2011) Rice A20/AN1 zinc-finger containing stress-associated proteins (SAP1/11) and a receptor-like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants. New Phytol 191:721–732

    CAS  PubMed  Google Scholar 

  • Gilles GC, Gervais ML, Planchet E, Satour P, Limami AM, Lelievre E (2011) A stress-associated protein containing A20/AN1 zing-finger domains expressed in Medicago truncatula seeds. Plant Physiol Biochem 49:303–310

    Google Scholar 

  • Grzybowska EA (2012) Human intronless genes: functional groups, associated diseases, evolution, and mRNA processing in absence of splicing. Biochem Biophys Res Commun 424:1–6

    CAS  PubMed  Google Scholar 

  • He X, Xie S, Xie P, Yao M, Liu W, Qin L, Liu Z, Zheng M, Liu H, Guan M (2019) Genome-wide identification of stress-associated proteins (SAP) with A20/AN1 zinc finger domains associated with abiotic stresses responses in Brassica napus. Environ Exp Bot 165:108–119

    CAS  Google Scholar 

  • Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479

    CAS  PubMed  Google Scholar 

  • Heyninck K, Beyaert R (2005) A20 inhibits NF-kappaB activation by dual ubiquitin-editing functions. Trends Biochem Sci 30:1–4

    CAS  PubMed  Google Scholar 

  • Hishiya A, Iemura S, Natsume T, Takayama S, Ikeda K, Watanbe K (2006) A novel ubiquitin-binding protein ZNF216 functioning in muscle atrophy. EMBO J 25:554–564

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hozain MD, Abdelmageed H, Lee J, Kang M, Fokar M, Allen RD, Holaday AS (2012) Expression of AtSAP5 in cotton upregulates putative stress-responsive genes and improves the tolerance to rapidly developing water deficit and moderate heat stress. J Plant Physiol 169:1261–1270

    CAS  PubMed  Google Scholar 

  • Huang J, Wang MM, Jiang Y, Bao YM, Xi H, Sun H, Xu QD, Lan XH, Zhang SH (2008) Expression analysis of rice A20/AN1-type zinc finger genes and characterization of ZFP177 that contributes to temperature stress tolerance. Gene 420:135–144

    CAS  PubMed  Google Scholar 

  • Hurley JH, Lee S, Prag G (2006) Ubiquitin-binding domains. Biochem J 399:361–372

    CAS  PubMed  PubMed Central  Google Scholar 

  • Irulappan V, Senthil-Kumar M (2018) Morpho-physiological traits and molecular intricacies associated with tolerance to combined drought and pathogen stress in plants. In: Gosal S, Wani S (eds) Biotechnologies of crop improvement, vol 3. Springer, Cham. https://doi.org/10.1007/978-3-319-94746-4_4

    Chapter  Google Scholar 

  • Jedmowski C, Ashoub A, Momtaz O, Brüggemann W (2015) Impact of drought, heat, and their combination on chlorophyll fluorescence and yield of wild barley (Hordeum spontaneum). J Bot 2015:120868

    Google Scholar 

  • Jia H, Li J, Zhang J, Ren Y, Hu J, Lu M (2016) Genome-wide survey and expression analysis of the stress-associated protein gene family in desert poplar, Populus euphratica. Tree Genet Genom. https://doi.org/10.1007/s11295-016-1033-8

    Article  Google Scholar 

  • Jin Y, Meng W, Junjie F, Ning X, Lian Z, Jia Y, Zheng Z, Guoying W (2007) Phylogenetic and expression analysis of ZnF-AN1 genes in plants. Genomics 90:265–275

    CAS  PubMed  Google Scholar 

  • Kang M, Abdelmageed H, Lee S, Reichert A, Mysore KS, Allen RD (2013) AtMBP-1, an alternative translation product of LOS2, affects abscisic acid responses and is modulated by the E3 ubiquitin ligase AtSAP5. Plant J 76:481–493

    CAS  PubMed  Google Scholar 

  • Kang M, Fokar M, Abdelmageed H, Allen RD (2011) Arabidopsis SAP5 functions as a positive regulator of stress responses and exhibits E3 ubiquitin ligase activity. Plant Mol Biol 75:451–466

    CAS  PubMed  Google Scholar 

  • Kang M, Lee S, Abdelmageed H, Reichert A, Lee HK, Fokar M, Mysore KS, Allen RD (2017) Arabidopsis stress associated protein 9 mediates biotic and abiotic stress responsive ABA signaling via the proteasome pathway. Plant Cell Environ 40:702–716

    CAS  PubMed  Google Scholar 

  • Kanneganti V, Gupta AK (2008) Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice. Plant Mol Biol 66:445–462

    CAS  PubMed  Google Scholar 

  • Kothari KS, Dansana PK, Giri J, Tyagi AK (2016) Rice stress associated protein 1 (OsSAP1) interacts with aminotransferase (OsAMTR1) and pathogenesis-related 1a protein (OsSCP) and regulates abiotic stress responses. Front Plant Sci 7:1057

    PubMed  PubMed Central  Google Scholar 

  • Kranner I, Minibayeva FV, Beckett RP, Seal CE (2010) What is stress? Concepts, definitions and applications in seed science. New Phytol 188:655–673

    CAS  PubMed  Google Scholar 

  • Lai W, Zhou Y, Pan R, Liao L, He J, Liu H, Yang Y, Liu S (2020) Identification and expression analysis of stress-associated proteins (SAPs) containing A20/AN1 zinc finger in cucumber. Plants 9:400

    CAS  PubMed Central  Google Scholar 

  • Lespinet O, Wolf YI, Koonin EV, Aravind L (2002) The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res 12:1048–1059

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Sun P, Xia Y, Zheng G, Sun J, Jia H (2019) A stress-associated protein, PtSAP13, from populus trichocarpa provides tolerance to salt stress. Int J Mol Sci 20:5782

    CAS  PubMed Central  Google Scholar 

  • Li W, Yi Wang, Li R, Chang X, Yuan X, Jing R (2021) Cloning and characterization of TaSAP7-A, a member of the stress-associated protein family in common wheat. Front Plant Sci. https://doi.org/10.3389/fpls.2021.609351

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu S, Wang J, Jiang S, Wang H, Gao Y, Zhang H, Li D, Song F (2019) Tomato SlSAP3, a member of the stress-associated protein family, is a positive regulator of immunity against Pseudomonas syringae pv. tomato DC3000. Mol Plant Pathol 20:815–830

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Yuan X, Wang Y, Wang H, Wang J, Shen Z, Gao Y, Li D, Song F (2018) Tomato stress-associated protein 4 contributes positively to immunity against necrotrophic fungus botrytis cinerea. Mol Plant Microbe Interact. https://doi.org/10.1094/mpmi-04-18-0097-r

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu J, Yang X, Yang X, Xu M, Liu J, Xue M, Ma P (2016) Isolation and characterization of LcSAP, a Leymus chinensis gene which enhances the salinity tolerance of Saccharomyces cerevisiae. Mol Biol Rep 44(1):5–9. https://doi.org/10.1007/s11033-016-4091-y

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Xu Y, Xiao J, Ma Q, Li D, Xue Z, Chong K (2011) OsDOG, a gibberellin-induced A20/AN1 zinc-finger protein, negatively regulates gibberellin-mediated cell elongation in rice. J Plant Physiol 168:1098–1105

    CAS  PubMed  Google Scholar 

  • Lloret A, Conejero A, Leida C, Petri C, Gil-Muñoz F, Burgos L, Badenes LM, Rios G (2017) Dual regulation of water retention and cell growth by a stress-associated protein (SAP) gene in Prunus. Sci Rep 7:332

    PubMed  PubMed Central  Google Scholar 

  • Lu TT, Onizawa M, Hammer GE, Turer EE, Yin Q, Damko E, Agelidis A, Shifrin N, Advincula R, Barrera J, Malynn BA, Wu H, Ma A (2013) Dimerization and ubiquitin mediated recruitment of A20, a complex deubiquitinating enzyme. Immunity 38:896–905

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma A, Malynn BA (2012) A20: linking a complex regulator of ubiquitylation to immunity and human disease. Nat Rev Immunol 12:774–785

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mauro C, Pacifico F, Livorgna A, Mellone S, Lannettu A, Acquaviva R, Formisano S, Vito P, Leonardi A (2006) ABIN-1 binds to NEMO/IKK gamma and co-operates with A20 in inhibiting NF-kappaB. J Biol Chem 281:18482–18488

    CAS  PubMed  Google Scholar 

  • McDermott MF, Aksentijevich I (2002) The autoinflammatory syndromes. Curr Opin Allergy Clin Immunol 2:511–516

    PubMed  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    CAS  PubMed  Google Scholar 

  • Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19

    CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    CAS  PubMed  Google Scholar 

  • Moore M, Gossmann N, Dietz K-J (2016) Redox regulation of cytosolic translation in plants. Trends Plant Sci 21:388–397

    CAS  PubMed  Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci USA 101:6309–6314

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muthuramalingam P, Jeyasri R, Selvaraj A, Kalaiyarasi D, Aruni W, Pandian STK, Manikandan R (2020) Global transcriptome analysis of novel stress associated protein (SAP) genes expression dynamism of combined abiotic stresses in Oryza sativa (L.): an in silico approach. J Biomol Struct Dyn. https://doi.org/10.1080/07391102.2020.1747548

    Article  PubMed  Google Scholar 

  • Nakamura N (2018) Ubiquitin system. Int J Mol Sci 19:1080

    PubMed Central  Google Scholar 

  • Ngo ST, Steyn FJ, McCombe PA (2014) Gender differences in autoimmune disease. Front Neuroendocrinol 35:347–369

    CAS  PubMed  Google Scholar 

  • Opipari AW, Boguski MS, Dixit VM (1990) The A20 cDNA induced by tumor necrosis factor alpha encodes a novel type of zinc finger protein. J Biol Chem 265:14705–14708

    CAS  PubMed  Google Scholar 

  • Pandey P, Ramegowda V, Senthil-Kumar M (2015a) Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms. Front Plant Sci 6:723

    PubMed  PubMed Central  Google Scholar 

  • Pandey P, Sinha R, Mysore KS, Senthil-Kumar M (2015) Impact of concurrent drought stress and pathogen infection on plants. In: Mahalingam R (ed) Combined stresses in plants. Springer, Cham. https://doi.org/10.1007/978-3-319-07899-1_10

    Chapter  Google Scholar 

  • Peckham D, Scambler T, Savic S, McDermott MF (2017) The burgeoning field of innate immune-mediated disease and autoinflammation. J Pathol 241:123–139

    CAS  PubMed  Google Scholar 

  • Petrov VD, Van Breusegem F (2012) Hydrogen peroxide—a central hub for information flow in plant cells. AoB Plants 2012:pls014

    PubMed  PubMed Central  Google Scholar 

  • Penengo L, Mapelli M, Murachelli AG, Confalonieri S, Magri L, Musacchio A, Fiore PPD, Schneider TR (2006) Crystal structure of the ubiquitin binding domains of Rabex-5 reveals two modes of interaction with ubiquitin. Cell 124(6):1183–1195. https://doi.org/10.1016/j.cell.2006.02.020

    Article  CAS  PubMed  Google Scholar 

  • Prasad PVV, Pisipati SR, Momcilovic I, Ristic Z (2011) Independent and combined effects of high temperature and drought stress during grain filling on plant yield and chloroplast EF-Tu expression in spring wheat. J Agron Crop Sci 197:430–441

    CAS  Google Scholar 

  • Prasch CM, Sonnewald U (2013) Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol 162:1849–1866

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ramu VS, Paramanantham A, Ramegowda V, Mohan-Raju B, Udayakumar M, Senthil-Kumar M (2016) Transcriptome analysis of sunflower genotypes with contrasting oxidative stress tolerance reveals individual- and combined- biotic and abiotic stress tolerance mechanisms. PLoS ONE 11:e0157522

    PubMed  PubMed Central  Google Scholar 

  • Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 37:1059–1073

    CAS  PubMed  Google Scholar 

  • Roos G, Messens J (2011) Protein sulfenic acid formation: from cellular damage to redox regulation. Free Radic Biol Med 51:314–326

    CAS  PubMed  Google Scholar 

  • Sharma G, Giri J, Tyagi A (2015) Rice OsiSAP7 negatively regulates ABA stress signaling and imparts sensitivity to water deficit stress in Arabidopsis. Plant Sci 237:80–92

    CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene network involved in drought stress tolerance and response. J Exp Bot 58:221–227

    CAS  PubMed  Google Scholar 

  • Sinha R, Gupta A, Senthil-Kumar M (2016) Understanding the impact of drought on foliar and xylem invading bacterial pathogen stress in chickpea. Front Plant Sci 7:902

    PubMed  PubMed Central  Google Scholar 

  • Solanke AU, Sharma MK, Tyagi AK, Sharma AK (2009) Characterization and phylogenetic analysis of environmental stress-responsive SAP gene family encoding A20/AN1 zinc finger proteins in tomato. Mol Genet Genom 282:153–164

    CAS  Google Scholar 

  • Sreedharan S, Shekhawat UK, Ganapathi TR (2012) MusaSAP1, a A20/AN1 zinc finger gene from banana functions as a positive regulator indifferent stress response. Plant Mol Biol 80:503–517

    CAS  PubMed  Google Scholar 

  • Ströher E, Wang XJ, Roloff N, Klein P, Husemann A, Dietz KJ (2009) Redox-dependent regulation of the stress-induced zinc-finger protein SAP12 in Arabidopsis thaliana. Mol Plant Pathol 2:357–367

    Google Scholar 

  • Takatsuji H (1999) Zinc-finger proteins: the classical zinc finger emerges in contemporary plant science. Plant Mol Biol 39:1073–1078

    CAS  PubMed  Google Scholar 

  • Thaura GH, Michael GS, Donaldo M, Denis F, Alexandra P, Walid BR, Rania BS, Satoshi O, Maria CR, Manabu I, Joe T, Abdullah AD, Emmanuel G, Afif H (2017) Expression of the Aeluropus littoralis AlSAP gene enhances rice yield under field drought at the reproductive stage. Front Plant Sci 8:994

    Google Scholar 

  • Tokunaga F, Nishimasu H, Ishitani R, Goto E, Noguchi T, Mio K, Kamei K, Ma A, Iwai K, Nureki O (2012) Specific recognition of linear polyubiquitin by A20 zinc finger 7 is involved in NF-kappaB regulation. EMBO J 31:3856–3870

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tyagi H, Jha S, Sharma M, Giri J, Tyagi AK (2014) Rice SAPs are responsive to multiple biotic stresses and overexpression of OsSAP1, an A20/AN1 zinc-finger protein, enhances the basal resistance against pathogen infection in tobacco. Plant Sci 225:68–76

    CAS  PubMed  Google Scholar 

  • Verhelst K, Carpentier I, Kreike M, Meloni L, Verstrepen L, Kensche T, Dikic I, Beyaert R (2012) A20 inhibits LUBAC-mediated NF-kappaB activation by binding linear polyubiquitin chains via its zinc finger 7. EMBO J 31:3845–3855

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vij S, Tyagi AK (2006) Genome-wide analysis of the stress associated protein (SAP) gene family containing A20/AN1 zinc-finger(s) in rice and their phylogenetic relationship with Arabidopsis. Molecular Genet Genom 276:565–575

    CAS  Google Scholar 

  • Vij S, Tyagi AK (2008) A20/AN1 zinc-finger domain-containing proteins in plants and animals represent common elements in stress response. Funct Integr Genom 8:301–307

    CAS  Google Scholar 

  • Wang Y, Zhang L, Zhang L, Xing T, Peng J, Sun S, Chen G, Wang X (2013) A novel stress-associated protein SbSAP14 from Sorghum bicolor confers tolerance to salt stress in transgenic rice. Mol Breed 32:437–449

    CAS  Google Scholar 

  • Wang Z, Kuang J, Han B, Chen S, Liu A (2020) Genomic characterization and expression profiles of stress-associated proteins (SAPs) in castor bean (Ricinus communis). Plant Divers. https://doi.org/10.1016/j.pld.2020.07.010

    Article  PubMed  PubMed Central  Google Scholar 

  • Wertz IE, O’Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S, Wu P, Wiesmann C, Baker R, Boone DL, Ma A, Eugene VK, Dixit MV (2004) De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430:694–699

    CAS  PubMed  Google Scholar 

  • Willems P, Mhamdi A, Stael S, Storme V, Kerchev P, Noctor G, Gevaert K, Van Breusegem F (2016) The ROS wheel: refining ROS transcriptional footprints. Plant Physiol 171:1720–1733

    PubMed  PubMed Central  Google Scholar 

  • Xiang-Zhan Z, Wei-Jun Z, Xin-You C, Xi-Yan C, Shu-Ping Z, Tai-Fei Y, Jun C, Yong-Bin Z, Ming C, Shou-Cheng C, Zhao-Shi X, You-Zhi M (2019) Genomic analysis of stress associated proteins in soybean and the role of GmSAP16 in abiotic stress responses in arabidopsis and soybean. Front Plant Sci 10:1453

    Google Scholar 

  • Xu Q, Mao X, Wang Y, Wang J, Xi Y, Jing R (2018) A wheat gene TaSAP17-D encoding an AN1/AN1 zinc finger protein improves salt stress tolerance in transgenic Arabidopsis. J Integr Agric 17:507–516

    CAS  Google Scholar 

  • Xuan N, Jin Y, Zhang H, Xie Y, Liu Y, Wang G (2011) A putative maize zinc-finger protein gene, ZmAN13, participates in abiotic stress response. Plant Cell Tissue Organ Cult 107:101–112

    CAS  Google Scholar 

  • Yoon SK, Bae EK, Lee H, Choi YI, Han M, Choi H, Kang KS, Park EJ (2018) Downregulation of stress-associated protein 1 (PagSAP1) increases salt stress tolerance in poplar (Populus alba × P. glandulosa). Trees 32:823–833

    CAS  Google Scholar 

  • Yvona M, Vileb D, Braultc V, Blanca S, van Munstera M (2017) Drought reduces transmission of Turnip yellows virus, an insect-vectored circulative virus. Virus Res 241:131–136

    Google Scholar 

  • Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang N, Yin Y, Liu X, Tong S, Xing J, Zhang Y, Pudake NR, Izquierdo ME, Peng M, Xin M, Hu Z, Ni Z, Sun Q, Yao Y (2017) The E3 ligase TaSAP5 alters drought stress responses by promoting the degradation of DRIP proteins. Plant Physiol 175:1878–1892

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XZ, Zheng WJ, Cao XY, Cui XY, Zhao SP, Yu TF, Chen J, Zhou BY, Chen M, Chai CS, Xu SZ, Ma YZ (2019) Genomic analysis of stress associated proteins in soybean and the role of GmSAP16 in abiotic stress responses in arabidopsis and soybean. Front Plant Sci. https://doi.org/10.3389/fpls.2019.01453

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Authors' research in this area was supported by the DST INSPIRE Faculty Grant of Department of Science & Technology (DST), Ministry of Science & Technology, Government of India (File No. DST/INSPIRE/04/2016/002341).

Author information

Author notes

  1. Varsa Shukla, Pooja Choudhary, Sumi Rana these authors have contributed equally to this work.

Authors and Affiliations

  1. Repository of Tomato Genomics Resources, Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad, Telangana, 500046, India

    Varsa Shukla, Pooja Choudhary, Sumi Rana & Mehanathan Muthamilarasan

Authors
  1. Varsa Shukla
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pooja Choudhary
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sumi Rana
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mehanathan Muthamilarasan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MM conceived and outlined the review; VS prepared the first draft, tables and figures; PC and SR critically revised the work and provided additional inputs. All the authors have read and approved the final version of the manuscript.

Corresponding author

Correspondence to Mehanathan Muthamilarasan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 198 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shukla, V., Choudhary, P., Rana, S. et al. Structural evolution and function of stress associated proteins in regulating biotic and abiotic stress responses in plants. J. Plant Biochem. Biotechnol. 30, 779–792 (2021). https://doi.org/10.1007/s13562-021-00704-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13562-021-00704-x

Keywords

Search

Navigation