Welcome to Acta Agronomica Sinica，Apr. 4, 2025

Acta Agron Sin ›› 2013, Vol. 39 ›› Issue (12): 2135-2144.doi: 10.3724/SP.J.1006.2013.02135

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Characteristics of PP2C Gene Family in Foxtail Millet (Setaria italica)

MIN Dong-Hong1,**,XUE Fei-Yang1,2,**,MA Ya-Nan1,2,CHEN Ming2,*,XU Zhao-Shi2,LI Lian-Cheng2,DIAO Xian-Min2,JIA Guan-Qing2,MA You-Zhi2   

  1. 1 College of Agronomy, Northwest A&F University / State Key Laboratory of Arid Region Crop Adversity Biology, Yangling 712100, China; 2 Institute of Crop Science, Chinese Academy of Agricultural Sciences / National Key Facility for Crop Gene Resources and Genetic Improvement / Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing 100081, China
  • Received:2013-05-13 Revised:2013-07-26 Online:2013-12-12 Published:2013-09-29

RichHTML

PDF

1352

Cited

2

Abstract:

PP2Cs are a group of monomeric serine/threonine protein phosphatases, which play an important role in regulation of hormone signaling pathways such as abscisic acid (ABA), jasmonic acid (JA) and salicylic acid (SA) in eukaryotes. In this study, we identified 80 candidate PP2C genes from foxtail millet genome via sequence alignment, and cluster analysis showed that PP2Cs in foxtail millet were divided into 12 subfamilies (subfamily A, B, C, D, E1, E2, F1, F2, G, H, I, and J). Foxtail millet and Arabidopsis share A, B, C, D, E1, E2, F1, F2, G, H, and I, while subfamily J is only in foxtail millet and subfamily L is only in Arabidopsis. Ten members of subfamily A in foxtail millet were named as SiPP2CA1–10, and gene expression profiles showed that the expression of these genes was induced by ABA, drought, high salt, cold and low nitrogen stresses. Among them, SiPP2CA6 and SiPP2CA8 showed high expression level in all treatments. Promoter analysis identified a variety of cis-acting elements involved in stress responses in promoter region of members in subfamily A, and a specific element responding to low nitrogen stress in SiPP2CA5, SiPP2CA6, SiPP2CA7, and SiPP2CA8. Further study demonstrated that SiPP2CA8mainly expressed in root, and its expression remained at high level under low nitrogen stress. Subcellular localization showed that SiPP2CA8 waslocalized in cytomembrane, cytoplasm and nucleus. Bimolecular fluorescence complementation (BiFC) assay demonstrated that SiPP2CA8 interacted with an ABA receptor like protein, SiRCAR3 (gene locus Si018317m.g), in cytomembrane, cytoplasm and nucleus. These results suggested that SiPP2CA8 may participate in ABA signaling pathway in foxtail millet.

Key words: Foxtail millet, PP2C gene family, Abiotic stress, Expression analysis

[1]Stern A, Privman E, Rasis M, Lavi S, Pupko T. Evolution of the metazoan protein phosphatase 2C superfamily. J Mol Evol, 2007, 64: 61–70



[2]Cohen P. The structure and regijlation of protein phosphatases. Ann Rev Biochem, 1989, 58: 453–508



[3]Schweighofer A, Hirt H, Meskiene I. Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci, 2004, 9: 236–243



[4]Meskiene I, Baudouin E, Schweighofer A, Liwosz A, Jonak C, Rodriguez P L, Jelinek H, Hirt H. Stress-induced protein phosphatase 2C is a negative regulator of a mitogen-activated protein kinase. J Biol Chem, 2003, 278: 18945–18952



[5]Shi Y G. Serine/threonine phosphatases: mechanism through structure. Cell, 2009, 139: 468–484



[6]Sheen J. Mutational analysis of protein phosphatase 2C involved in abscisic acid signal transduction in higher plants. Proc Natl Acad Sci USA, 1998, 95: 975–980



[7]Schweighofer A, Kazanaviciute V, Scheikl E, Teige M, Doczi R, Hirt H, Schwanninger M, Kant M, Schuurink R, Mauch F, Buchala A, Cardinale F, Meskiene I. The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. Plant Cell, 2007, 19: 2213–2224



[8]Nishimura N, Okamoto M, Narusaka M, Yasuda M, Nakashita H, Shinozaki K, Narusaka Y, Hirayama T. ABA hypersensitive germination2-1 causes the activation of both abscisic acid and salicylic acid responses in Arabidopsis. Plant Cell Physiol, 2009, 50: 2112–2122



[9]Hirayama T, Shinozaki K. Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci, 2007, 12: 343–351



[10]Meyer K, Leube M P, Grill E. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science, 1994, 264: 1452–1455



[11]Jeffrey Leung S M, and Jérôme Giraudat. The Arabidopsis ABSCISIC ACID-INSENSlTIVE2 (AB12) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell, 1997, 9: 759–771



[12]Angela Saez N A, Miguel Gonzalez Guzman, Mary Paz Gonzalez-Garcia, Carlos Nicolas, Oscar Lorenzo, Pedro L Rodriguez. Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J, 2004, 37: 354–369



[13]Yoshida T, Nishimura N, Kitahata N, Kuromori T, Ito T, Asami T, Shinozaki K, Hirayama T. ABA-hypersensitive germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol, 2006, 140: 115–126



[14]Nishimura N, Yoshida T, Kitahata N, Asami T, Shinozaki K, Hirayama T. ABA-Hypersensitive Germination1 encodes a protein phosphatase 2C, an essential component of abscisic acid signaling in Arabidopsis seed. Plant J, 2007, 50: 935–949



[15]Reyes D, Rodriguez D, Gonzalez-Garcia M P, Lorenzo O, Nicolas G, Garcia-Martinez J L, Nicolas C. Overexpression of a protein phosphatase 2C from beech seeds in Arabidopsis shows phenotypes related to abscisic acid responses and gibberellin biosynthesis. Plant Physiol, 2006, 141: 1414–1424



[16]Saavedra X, Modrego A, Rodriguez D, Gonzalez-Garcia M P, Sanz L, Nicolas G, Lorenzo O. The nuclear interactor PYL8/RCAR3 of Fagus sylvatica FsPP2C1 is a positive regulator of abscisic acid signaling in seeds and stress. Plant Physiol, 2010, 152: 133–150



[17]Liu L, Hu X, Song J, Zong X, Li D, Li D. Over-expression of a Zea mays L. protein phosphatase 2C gene (ZmPP2C) in Arabidopsis thaliana decreases tolerance to salt and drought. J Plant Physiol, 2009, 166: 531–542



[18]Liu X, Zhu Y, Zhai H, Cai H, Ji W, Luo X, Li J, Bai X. AtPP2CG1, a protein phosphatase 2C, positively regulates salt tolerance of Arabidopsis in abscisic acid-dependent manner. Biochem Biophys Res Commun, 2012, 422: 710–715



[19]Jia H F, Lu D, Sun J H, Li C L, Xing Y, Qin L, Shen Y Y. Type 2C protein phosphatase ABI1 is a negative regulator of strawberry fruit ripening. J Exp Bot, 2013 (DOI:10.1093/jxb/ert1028)



[20]Xue T T, Wang D, Zhang S Z, Ehlting J, Ni F, Jakab S, Zheng C C, Zhong Y. Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis. BMC Genom, 2008, 9: 550



[21]Bhaskara G B, Nguyen T T, Verslues P E. Unique drought resistance functions of the highly ABA-induced clade A protein phosphatase 2Cs. Plant Physiol, 2012, 160: 379–395



[22]Wang Z M, Devos K M, Liu C J, Wang R Q, Gale M D. Construction of RFLP-based maps of foxtail millet, Setaria italica (L.) P. Beauv. Theor Appl Genet, 1998, 96: 31–36



[23]Doust A N, Kellogg E A, Devos K M, Bennetzen J L. Foxtail millet: a sequence-driven grass model system. Plant Physiol, 2009, 149: 137–141



[24]Bennetzen J L, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli A C, Estep M, Feng L, Vaughn J N, Grimwood J, Jenkins J, Barry K, Lindquist E, Hellsten U, Deshpande S, Wang X W, Wu X M, Mitros T, Triplett J, Yang X H, Ye C Y, Mauro-Herrera M, Wang L, Li P, Sharma M, Sharma R, Ronald P C, Panaud O, Kellogg E A, Brutnell T P, Doust A N, Tuskan G A, Rokhsar D, Devos K M. Reference genome sequence of the model plant Setaria. Nat Biotechnol, 2012, 30: 555–561



[25]Zhang G Y, Liu X, Quan Z W, Cheng S F, Xu X, Pan S K, Xie M, Zeng P, Yue Z, Wang W L, Tao Y, Bian C, Han C L, Xia Q J, Peng X H, Cao R, Yang X H, Zhan D L, Hu J C, Zhang Y X, Li H N, Li H, Li N, Wang J Y, Wang C C, Wang R Y, Guo T, Cai Y J, Liu C Z, Xiang H T, Shi Q X, Huang P, Chen Q C, Li Y R, Wang J, Zhao Z H, Wang J. Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat Biotechnol, 2012, 30: 549–554



[26]Yoo S D, Cho Y H, Sheen J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Prot, 2007, 2: 1565–1572



[27]Loppes R, Radoux M. Abscisic acid biosynthesis and catabolism. Ann Rev Plant Biol, 2005, 56: 165–185



[28]Lim C W, Kim J H, Baek W, Kim B S, Lee S C. Functional roles of the protein phosphatase 2C, AtAIP1, in abscisic acid signaling and sugar tolerance in Arabidopsis. Plant Sci, 2012, 187: 83–88



[29]Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science, 2009, 324: 1064–1068
[1] CHEN Song-Yu, DING Yi-Juan, SUN Jun-Ming, HUANG Deng-Wen, YANG Nan, DAI Yu-Han, WAN Hua-Fang, QIAN Wei. Genome-wide identification of BnCNGC and the gene expression analysis in Brassica napus challenged with Sclerotinia sclerotiorum and PEG-simulated drought [J]. Acta Agronomica Sinica, 2022, 48(6): 1357-1371.
[2] JIN Min-Shan, QU Rui-Fang, LI Hong-Ying, HAN Yan-Qing, MA Fang-Fang, HAN Yuan-Huai, XING Guo-Fang. Identification of sugar transporter gene family SiSTPs in foxtail millet and its participation in stress response [J]. Acta Agronomica Sinica, 2022, 48(4): 825-839.
[3] DU Xiao-Fen, WANG Zhi-Lan, HAN Kang-Ni, LIAN Shi-Chao, LI Yu-Xin, ZHANG Lin-Yi, WANG Jun. Identification and analysis of RNA editing sites of chloroplast genes in foxtail millet [Setaria italica (L.) P. Beauv.] [J]. Acta Agronomica Sinica, 2022, 48(4): 873-885.
[4] WU Yan-Fei, HU Qin, ZHOU Qi, DU Xue-Zhu, SHENG Feng. Genome-wide identification and expression analysis of Elongator complex family genes in response to abiotic stresses in rice [J]. Acta Agronomica Sinica, 2022, 48(3): 644-655.
[5] ZHAO Mei-Cheng, DIAO Xian-Min. Phylogeny of wild Setaria species and their utilization in foxtail millet breeding [J]. Acta Agronomica Sinica, 2022, 48(2): 267-279.
[6] WANG Yan-Peng, LING Lei, ZHANG Wen-Rui, WANG Dan, GUO Chang-Hong. Genome-wide identification and expression analysis of B-box gene family in wheat [J]. Acta Agronomica Sinica, 2021, 47(8): 1437-1449.
[7] LI Wen-Lan, LI Wen-Cai, SUN Qi, YU Yan-Li, ZHAO Meng, LU Shou-Ping, LI Yan-Jiao, MENG Zhao-Dong. A study of expression pattern of auxin response factor family genes in maize (Zea mays L.) [J]. Acta Agronomica Sinica, 2021, 47(6): 1138-1148.
[8] YIN Ming, YANG Da-Wei, TANG Hui-Juan, PAN Gen, LI De-Fang, ZHAO Li-Ning, HUANG Si-Qi. Genome-wide identification of GRAS transcription factor and expression analysis in response to cadmium stresses in hemp (Cannabis sativa L.) [J]. Acta Agronomica Sinica, 2021, 47(6): 1054-1069.
[9] MA Gui-Fang, MAN Xia-Xia, ZHANG Yi-Juan, GAO Hao, SUN Zhao-Xia, LI Hong-Ying, HAN Yuan-Huai, HOU Si-Yu. Integrated analysis between folate metabolites profiles and transcriptome of panicle in foxtail millet [J]. Acta Agronomica Sinica, 2021, 47(5): 837-846.
[10] JIA Xiao-Ping, LI Jian-Feng, ZHANG Bo, QUAN Jian-Zhang, WANG Yong-Fang, ZHAO Yuan, ZHANG Xiao-Mei, WANG Zhen-Shan, SANG Lu-Man, DONG Zhi-Ping. Responsive features of SiPRR37 to photoperiod and temperature, abiotic stress and identification of its favourable allelic variations in foxtail millet (Setaria italica L.) [J]. Acta Agronomica Sinica, 2021, 47(4): 638-649.
[11] YUE Jie-Ru, BAI Jian-Fang, ZHANG Feng-Ting, GUO Li-Ping, YUAN Shao-Hua, LI Yan-Mei, ZHANG Sheng-Quan, ZHAO Chang-Ping, ZHANG Li-Ping. Cloning and potential function analysis of ascorbic peroxidase gene of hybrid wheat in seed aging [J]. Acta Agronomica Sinica, 2021, 47(3): 405-415.
[12] MENG Yu-Yu, WEI Chun-Ru, FAN Run-Qiao, YU Xiu-Mei, WANG Xiao-Dong, ZHAO Wei-Quan, WEI Xin-Yan, KANG Zhen-Sheng, LIU Da-Qun. TaPP2-A13 gene shows induced expression pattern in wheat responses to stresses and interacts with adaptor protein SKP1 from SCF complex [J]. Acta Agronomica Sinica, 2021, 47(2): 224-236.
[13] HE Xiao, LIU Xing, XIN Zheng-Qi, XIE Hai-Yan, XIN Yu-Feng, WU Neng-Biao. Molecular cloning, expression, and enzyme kinetic analysis of a phenylalanine ammonia-lyase gene in Pinellia ternate [J]. Acta Agronomica Sinica, 2021, 47(10): 1941-1952.
[14] JIA Xiao-Ping,YUAN Xi-Lei,LI Jian-Feng,WANG Yong-Fang,ZHANG Xiao-Mei,ZHANG Bo,QUAN Jian-Zhang,DONG Zhi-Ping. Photo-thermal interaction model under different photoperiod-temperature conditions and expression analysis of SiCCT gene in foxtail millet (Setaria italica L.) [J]. Acta Agronomica Sinica, 2020, 46(7): 1052-1062.
[15] LI Guo-Ji, ZHU Lin, CAO Jin-Shan, WANG You-Ning. Cloning and functional analysis of GmNRT1.2a and GmNRT1.2b in soybean [J]. Acta Agronomica Sinica, 2020, 46(7): 1025-1032.
Viewed
Full text
218
HTML PDF
Just accepted Online first Issue Just accepted Online first Issue
0 0 0 0 0 218

  From Others local
  Times 17 201
  Rate 8% 92%

Abstract
442
Just accepted Online first Issue
0 0 442
  From Others local
  Times 71 371
  Rate 16% 84%

Cited
Web of Science  Crossref   ScienceDirect  Search for Citations in Google Scholar >>
 
This page requires you have already subscribed to WoS.
  Shared   
  Discussed   
No Suggested Reading articles found!
Add: No. 80 Xueyuan South Rd, Beijing 100081, P. R. China E-mail: zwxb301@caas.cn
Supported by Beijing Magtech Co.Ltd