Skip to main content
Log in

Genome-wide identification and characterization of cystatin family genes in rice (Oryza sativa L.)

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key messeage

11 Cystatin genes in rice were identified, and their expression patterns were comprehensively analyzed, which reveals multiple roles in both seed development and plant response to environmental variations.

Abstract

Cystatin is a group of small proteins and known to inhibit the activities of cysteine proteases in the papain C1A and legumain C13 peptidase families in plants. Cystatin family genes have only been well characterized recently in a few plant species such as Hordeum vulgare and Nicotiana tabacum, which show their critical roles in programmed cell death and responses to biotic stresses. Up to now, little is known about cystatin family genes and their roles in Oryza sativa, a model plant for cereal biology study. Here, we identified 11 cystatin genes in rice genome. Comprehensive expression profile analysis reveals that cystatin family genes in rice display diverse expression pattern. They are temporally regulated at different developmental stages during the process of seed production and germination. Our experiments also reveal that the majority of cystatin genes are responsive to plant hormones and different environmental cues including cold, drought and other abiotic stresses, while some others are very stable under different stresses, indicating their fundamental roles in normal plant development. In addition, their distribution in rice chromosomes and their evolutionary relation to the members of Cystatin family in A. thaliana and N. tabacum have also been analyzed. These works suggest multiple roles of cystatin family genes in both seed development and plant response to environmental variations.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alvarez-Fernandez M, Barrett AJ, Gerhartz B, Dando PM, Ni J, Abrahamson M (1999) Inhibition of mammalian legumain by some cystatins is due to a novel second reactive site. J Biol Chem 274:19195–19203

    Article  CAS  PubMed  Google Scholar 

  • Arai S, Watanabe H, Kondo H, Emori Y, Abe K (1991) Papain-inhibitory activity of oryzacystatin, a rice seed cysteine proteinase inhibitor, depends on the central Gln-Val-Val-Ala-Gly region conserved among cystatin superfamily members. J Biochem 109:294–298

    CAS  PubMed  Google Scholar 

  • Belenghi B, Acconcia F, Trovato M, Perazzolli M, Bocedi A, Polticelli F, Ascenzi P, Delledonne M (2003) AtCYS1, a cystatin from Arabidopsis thaliana, suppresses hypersensitive cell death. Euro J Biochem/FEBS 270:2593–2604

    Article  CAS  Google Scholar 

  • Christoff AP, Margis R (2014) The diversity of rice phytocystatins. Mol Genet Genomics 289:1321–1330

    Article  CAS  PubMed  Google Scholar 

  • Corr-Menguy F, Cejudo FJ, Mazubert C, Vidal J, Lelandais-Briere C, Torres G, Rode A, Hartmann C (2002) Characterization of the expression of a wheat cystatin gene during caryopsis development. Plant Mol Biol 50:687–698

    Article  PubMed  Google Scholar 

  • Deng H, Liu H, Li X, Xiao J, Wang S (2012) A CCCH-type zinc finger nucleic acid-binding protein quantitatively confers resistance against rice bacterial blight disease. Plant Physiol 158:876–889

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Du B, Zhang W, Liu B, Hu J, Wei Z, Shi Z, He R, Zhu L, Chen R, Han B, He G (2009) Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc Natl Acad Sci USA 106:22163–22168

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Goulet MC, Dallaire C, Vaillancourt LP, Khalf M, Badri AM, Preradov A, Duceppe MO, Goulet C, Cloutier C, Michaud D (2008) Tailoring the specificity of a plant cystatin toward herbivorous insect digestive cysteine proteases by single mutations at positively selected amino acid sites. Plant Physiol 146:1010–1019

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gutierrez-Campos R, Torres-Acosta JA, Saucedo-Arias LJ, Gomez-Lim MA (1999) The use of cysteine proteinase inhibitors to engineer resistance against potyviruses in transgenic tobacco plants. Nat Biotechnol 17:1223–1226

    Article  CAS  PubMed  Google Scholar 

  • Hong JK, Hwang JE, Lim CJ, Yang KA, Jin ZL, Kim CY, Koo JC, Chung WS, Lee KO, Lee SY, Cho MJ, Lim CO (2007) Over-expression of Chinese cabbage phytocystatin 1 retards seed germination in Arabidopsis. Plant Sci 172:556–563

    Article  CAS  Google Scholar 

  • Hu J, Wang K, Huang W, Liu G, Gao Y, Wang J, Huang Q, Ji Y, Qin X, Wan L, Zhu R, Li S, Yang D, Zhu Y (2012) The rice pentatricopeptide repeat protein RF5 restores fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GRP162. Plant Cell 24:109–122

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hwang JE, Hong JK, Je JH, Lee KO, Kim DY, Lee SY, Lim CO (2009) Regulation of seed germination and seedling growth by an Arabidopsis phytocystatin isoform, AtCYS6. Plant Cell Rep 28:1623–1632

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hwang JE, Hong JK, Lim CJ, Chen H, Je J, Yang KA, Kim DY, Choi YJ, Lee SY, Lim CO (2010) Distinct expression patterns of two Arabidopsis phytocystatin genes, AtCYS1 and AtCYS2, during development and abiotic stresses. Plant Cell Rep 29:905–915

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Do Choi Y, Kim M, Reuzeau C, Kim JK (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Koiwa H, Shade RE, Zhu-Salzman K, D’Urzo MP, Murdock LL, Bressan RA, Hasegawa PM (2000) A plant defensive cystatin (soyacystatin) targets cathepsin L-like digestive cysteine proteinases (DvCALs) in the larval midgut of western corn rootworm (Diabrotica virgifera virgifera). FEBS Lett 471:67–70

    Article  CAS  PubMed  Google Scholar 

  • Konrad R, Ferry N, Gatehouse AM, Babendreier D (2008) Potential effects of oilseed rape expressing oryzacystatin-1 (OC-1) and of purified insecticidal proteins on larvae of the solitary bee Osmia bicornis. PLoS One 3:e2664

    Article  PubMed Central  PubMed  Google Scholar 

  • Kouzuma Y, Inanaga H, Doi-Kawano K, Yamasaki N, Kimura M (2000) Molecular cloning and functional expression of cDNA encoding the cysteine proteinase inhibitor with three cystatin domains from sunflower seeds. J Biochem 128:161–166

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Fan C, Xing Y, Jiang Y, Luo L, Sun L, Shao D, Xu C, Li X, Xiao J, He Y, Zhang Q (2011) Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet 43:1266–1269

    Article  CAS  PubMed  Google Scholar 

  • Luo D, Xu H, Liu Z, Guo J, Li H, Chen L, Fang C, Zhang Q, Bai M, Yao N, Wu H, Wu H, Ji C, Zheng H, Chen Y, Ye S, Li X, Zhao X, Li R, Liu YG (2013) A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45:573–577

    Article  CAS  PubMed  Google Scholar 

  • Ma L, Xin H, Qu L, Zhao J, Yang L, Zhao P, Sun M (2011) Transcription profile analysis reveals that zygotic division results in uneven distribution of specific transcripts in apical/basal cells of tobacco. PLoS One 6:e15971

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martínez M, Díaz I (2008) The origin and evolution of plant cystatins and their target cysteine proteinases indicate a complex functional relationship. BMC Evol Biol 8:198

    Article  PubMed Central  PubMed  Google Scholar 

  • Martínez M, Abraham Z, Carbonero P, Díaz I (2005a) Comparative phylogenetic analysis of cystatin gene families from arabidopsis, rice and barley. Mol Gen Genomics 273:423–432

    Article  Google Scholar 

  • Martínez M, Rubio-Somoza I, Fuentes R, Lara P, Carbonero P, Díaz I (2005b) The barley cystatin gene (Icy) is regulated by DOF transcription factors in aleurone cells upon germination. J Exp Bot 56:547–556

    Article  PubMed  Google Scholar 

  • Martínez M, Díaz-Mendoza M, Carrillo L, Díaz I (2007) Carboxy terminal extended phytocystatins are bifunctional inhibitors of papain and legumain cysteine proteinases. FEBS Lett 581:2914–2918

    Article  PubMed  Google Scholar 

  • Martínez M, Cambra I, Carrillo L, Díaz-Mendoza M, Díaz I (2009) Characterization of the entire cystatin gene family in barley and their target cathepsin L-like cysteine-proteases, partners in the hordein mobilization during seed germination. Plant Physiol 151:1531–1545

    Article  PubMed Central  PubMed  Google Scholar 

  • Muntz K, Shutov AD (2002) Legumains and their functions in plants. Trends Plant Sci 7:340–344

    Article  CAS  PubMed  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    Article  CAS  PubMed  Google Scholar 

  • Seo YS, Chern M, Bartley LE, Han M, Jung KH, Lee I, Walia H, Richter T, Xu X, Cao P, Bai W, Ramanan R, Amonpant F, Arul L, Canlas PE, Ruan R, Park CJ, Chen X, Hwang S, Jeon JS, Ronald PC (2011) Towards establishment of a rice stress response interactome. PLoS Genet 7:e1002020

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Solomon M, Belenghi B, Delledonne M, Menachem E, Levine A (1999) The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11:431–444

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • van der Linde K, Hemetsberger C, Kastner C, Kaschani F, van der Hoorn RA, Kumlehn J, Doehlemann G (2012) A maize cystatin suppresses host immunity by inhibiting apoplastic cysteine proteases. Plant Cell 24:1285–1300

    Article  PubMed Central  PubMed  Google Scholar 

  • Xia K, Liu T, Ouyang J, Wang R, Fan T, Zhang M (2011) Genome-wide identification, classification, and expression analysis of autophagy-associated gene homologues in rice (Oryza sativa L.). DNA Res Int J Rapid Publ Rep Genes Genomes 18:363–377

    CAS  Google Scholar 

  • Yang J, Zhao X, Cheng K, Du H, Ouyang Y, Chen J, Qiu S, Huang J, Jiang Y, Jiang L, Ding J, Wang J, Xu C, Li X, Zhang Q (2012) A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science 337:1336–1340

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Liu S, Takano T (2008) Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance. Plant Mol Biol 68:131–143

    Article  CAS  PubMed  Google Scholar 

  • Zhao P, Zhou XM, Zhang LY, Wang W, Ma LG, Yang LB, Peng XB, Bozhkov PV, Sun MX (2013) A bipartite molecular module controls cell death activation in the Basal cell lineage of plant embryos. PLoS Biol 11:e1001655

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao P, Zhou XM, Zou J, Wang W, Wang L, Peng XB, Sun MX (2014) Comprehensive analysis of cystatin family genes suggests their putative functions in sexual reproduction, embryogenesis, and seed formation. J Exp Bot 65:5093–5107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work is supported by “973” project (2013CB126900) and NSFC project (31400171).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Meng-xiang Sun.

Additional information

Communicated by K. Chong.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 2234 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, W., Zhao, P., Zhou, Xm. et al. Genome-wide identification and characterization of cystatin family genes in rice (Oryza sativa L.). Plant Cell Rep 34, 1579–1592 (2015). https://doi.org/10.1007/s00299-015-1810-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-015-1810-0

Keywords

Navigation