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Journal of Integrative Agriculture  2020, Vol. 19 Issue (6): 1609-1624    DOI: 10.1016/S2095-3119(20)63181-1
Special Issue: 园艺-分子生物合辑Horticulture — Genetics · Breeding
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
Genome-wide identification and expression analysis of StPP2C gene family in response to multiple stresses in potato (Solanum tuberosum L.)
WANG Yi-fan1, LIAO Yu-qiu1, WANG Ya-peng3, YANG Jiang-wei1, 2, ZHANG Ning1, SI Huai-jun1, 2 
1 College of Life Science and Technology, Gansu Agricultural University, Lanzhou 730070, P.R.China
2 Gansu Provincial Key Laboratory of Aridland Crop Science, Gansu Agricultural University, Lanzhou 730070, P.R.China
3 College of Agronomy, Gansu Agricultural University, Lanzhou 730070, P.R.China
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The plant protein phosphatase 2Cs (PP2Cs) play an essential role in response to stress and abscisic acid (ABA) signaling pathway.  However, to date, no systemic characterization of the PP2Cs has yet been conducted in potato (Solanum tuberosum L.).  In the study, a comprehensive research was performed on genome-wide identification and expression analysis of StPP2C genes in potato.  A total of 78 potato StPP2C genes were identified based on specific structure of PP2C domain, which were distributed across 11 out of 12 potato chromosomes and divided into 12 (A–L) phylogenetic branches.  The result from gene duplication analysis showed that 14 StPP2Cs were involved in gene tandem duplication and 8 genes formed fragment duplication events, which indicated that both tandem and fragment duplication contributed to the expansion of the gene family in evolution.  Exon–intron structural analysis showed that they had a wide range of exon numbers.  Analysis of protein conservative motif demonstrated that StPP2Cs contained more similar motif structures in the same phylogenetic branches.  The cis-elements in StPP2C gene promoter regions were mainly responded to light, phytohormone and abiotic stress.  Most of them exhibited tissue-specific expression patterns, and some members could differentially express under abiotic stress.  The evidence suggested that StPP2C genes may contribute to different functions in several physiological stress and environmental stress conditions.  This study could provide new insights to further investigate StPP2C functional characteristics responding to various stresses in potato.
Keywords:  protein phosphatase 2C        expression pattern        stress        ABA        potato  
Received: 02 September 2019   Accepted:
Fund: This research was supported by the National Natural Science Foundation of China (31660416 and 31560413) and the Potato Industry Technology System of Gansu Province, China (GARS-03-P1).
Corresponding Authors:  Correspondence SI Huai-jun, Tel/Fax: +86-931-7631875, E-mail:   
About author:  WANG Yi-fan, Mobile: +86-18894312278, E-mail:;

Cite this article: 

WANG Yi-fan, LIAO Yu-qiu, WANG Ya-peng, YANG Jiang-wei, ZHANG Ning, SI Huai-jun. 2020. Genome-wide identification and expression analysis of StPP2C gene family in response to multiple stresses in potato (Solanum tuberosum L.). Journal of Integrative Agriculture, 19(6): 1609-1624.

Allen G J, Kuchitsu K, Chu S P, Murata Y, Schroeder J I. 1999. Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisic acid-induced cytoplasmic calcium rises in guard cells. The Plant Cell, 11, 1785–1798.
Antoni R, Gonzalez-Guzman M, Rodriguez L, Peirats-Llobet M, Pizzio G A, Fernandez M A, De Winne N, De Jaeger G, Dietrich D, Bennett M J, Rodriguez P L. 2013. PYRABACTIN RESISTANCE1-LIKE8 plays an important role for the regulation of abscisic acid signaling in root. Plant Physiology, 161, 931–941.
Antoni R, Gonzalez-Guzman M, Rodriguez L, Rodrigues A, Pizzio G A, Rodriguez P L. 2012. Selective inhibition of clade a phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors. Plant Physiology, 158, 970–980.
Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, de Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E, Grosdidier A, Hernandez C, Ioannidis V, Kuznetsov D, Liechti R, Moretti S, Mostaguir K, Redaschi N, Rossier G, Xenarios I, et al. 2012. Expasy: SIB bioinformatics resource portal. Nucleic Acids Research, 40, W597–W630.
Bailey T L, Boden M, Buske F A, Frith M, Grant C E, Clementi L, Ren J, Li W W, Noble W S. 2009. MEME Suite: Tools for motif discovery and searching. Nucleic Acids Research, 37, W202–W208.
Baril C, Sahmi M, Ashton-Beaucage D, Stronach B, Therrien M. 2008. The PP2C Alphabet is a negative regulator of stress-activated protein kinase signaling in Drosophila. Genetics, 181, 567–579.
Brandt B, Brodsky D E, Xue S, Negi J, Iba K, Kangasjarvi J, Ghassemian M, Stephan A B, Hu H, Schroeder J I. 2012. Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proceedings of the National Academy of Sciences of the United States of America, 109, 10593–10598.
Brody M S, Stewart V, Price C W. 2010. Bypass suppression analysis maps the signaling pathway within a multidomain protein: The RsbP energy stress phosphatase 2C from Bacillus subtilis. Molecular Microbiology, 72, 1221–1234.
Cao J M, Jiang M, Li P, Chu Z Q. 2016. Genome-wide identification and evolutionary analyses of the PP2C gene family with their expression profiling in response to multiple stresses in Brachypodium distachyon. BMC Genomics, 17, 175.
Chen C, Yu Y, Ding X, Liu B, Duanmu H, Zhu D, Sun X, Cao L, Zaib-Un-Nisa, Li Q, Zhu Y. 2017. Genome-wide analysis and expression profiling of PP2C clade D under saline and alkali stresses in wild soybean and Arabidopsis. Protoplasm, 255, 643–654.
Chernoff J. 1999. Protein tyrosine phosphatases as negative regulators of mitogenic signaling. Journal of Cellular Physiology, 180, 173.
Cohen P. 2003. The structure and regulation of protein phosphatases. Annual Review of Biochemistry, 58, 453.
Cohen P T. 1997. Novel protein serine/threonine phosphatases: Variety is the spice of life. Trends in Biochemical Sciences, 22, 245–251.
Corton J M, Gillespie J G, Hardie D G. 1994. Role of the AMP-activated protein kinase in the cellular stress response. Current Biology, 4, 315–324.
Couto D, Niebergall R, Liang X X, Bücherl C A, Sklenar J,  Macho A P, Ntoukakis V, Derbyshire P, Altenbach D, Maclean D, Robatzek S, Uhrig J, Menke F, Zhou J M, Zipfel C. 2016. The Arabidopsis protein phosphatase PP2C38 negatively regulates the central immune kinase BIK1. PLoS Pathogens, 12, e1005811.
Galbiati M, Simoni L, Pavesi G, Cominelli E, Francia P, Vavasseur A, Nelson T, Bevan M, Tonelli C. 2008. Gene trap lines identify Arabidopsis genes expressed in stomatal guard cells. The Plant Journal, 53, 750–762.
Goldsbrough A P, Albrecht H, Stratford R. 1993. Salicylic acid-inducible binding of a tobacco nuclear protein to a 10 bp
sequence which is highly conserved amongst stress-inducible genes. The Plant Journal, 3, 563–571.
González A, Ruiz A, Serrano R, Ariño J, Casamayor A. 2006. Transcriptional profiling of the protein phosphatase 2C family in yeast provides insights into the unique functional roles of Ptc1. Journal of Biological Chemistry, 281, 35057–35069.
Gu Z L, Cavalcanti A, Chen F C, Bouman P, Li W H. 2002. Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Molecular Biology and Evolution, 19, 256–262.
Han L, Li J, Jin M, Su Y. 2018. Functional analysis of a type 2C protein phosphatase gene from Ammopiptanthus mongolicus. Gene, 653, 29–42.
den Hertog J. 1999. Protein-tyrosine phosphatases in development. Mechanisms of Development, 85, 3–14.
Hirayama T, Umezawa T. 2010. PP2C-SnRK2 complex: The central regulator of an abscisic acid signaling pathway. Plant Signaling Behavior, 5, 160–163.
Hu B, Jin J, Guo A Y, Zhang H, Luo J, Gao G. 2014. GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics, 31, 1296–1297.
Jiang J Z, Zhang W, Guo Z X, Cai C C, Su Y L, Wang R X, Wang J Y. 2011. Functional annotation of an expressed sequence tag library from Haliotis diversicolor and analysis of its plant-like sequences. Marine Genomics, 4, 189–196.
Kent W J, Baertsch R, Hinrichs A, Miller W, Haussler D. 2003. Evolution’s cauldron: Duplication, deletion, and rearrangement in the mouse and human genomes. Proceedings of the National Academy of Sciences of the United States of America, 100, 11484–11489.
Kerk D, Bulgrien J, Smith D W, Barsam B, Veretnik S, Gribskov M. 2002. The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis. Plant Physiology, 129, 908–925.
Kong H, Landherr L L, Frohlich M W, Leebens-Mack J, Ma H, de Pamphilis C W. 2007. Patterns of gene duplication in the plant SKP1 gene family in angiosperms: Evidence for multiple mechanisms of rapid gene birth. The Plant Journal, 50, 873–885.
Lee M W, Jelenska J, Greenberg J T. 2008. Arabidopsis proteins important for modulating defense responses to Pseudomonas syringae that secrete HopW1-1. The Plant Journal, 54, 452–465.
Lee T H, Tang H, Wang X, Paterson A H. 2013. PGDD: A database of gene and genome duplication in plants. Nucleic Acids Research, 41, D1152–D1158.
Li Y S, Sun H, Wang Z F, Duan M, Huang S D, Yang J, Huang J, Zhang H S. 2013. A novel nuclear protein phosphatase 2C negatively regulated by ABI1 is involved in abiotic stress and panicle development in rice. Molecular Biotechnology, 54, 703–710.
Liu L, Xu W, Hu X, Liu H, Lin Y. 2016. W-box and G-box elements play important roles in early senescence of rice flag leaf. Scientific Reports, 6, 20881.
MacKintosh C, Coggins J, Cohen P. 1991. Plant protein phosphatases subcellular distribution, detection of protein phosphatase 2C and identification of protein phosphatase 2A as the major quinate dehydrogenase phosphatase. Biochemical Journal, 273, 733–738.
Mattick J S, Gagen M J. 2001. The evolution of controlled multitasked gene networks: The role of introns and other noncoding RNAs in the development of complex organisms. Molecular Biology and Evolution, 18, 1611–1630.
Mehan M R, FreimerN B, Ophoff R A. 2004. A genome-wide survey of segmental duplications that mediate common human genetic variation of chromosomal architecture. Human Genomics, 1, 335–344.
Menges M, Hennig L, Gruissem W, Murray J A. 2002. Cell cycle-regulated gene expression in Arabidopsis. Journal of Biological Chemistry, 277, 41987–42002.
Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J. 2001. The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. The Plant Journal, 25, 295–303.
Mitula F, Tajdel M, Cie?la A, Kasprowicz-Malu?ki A, Kulik A, Babula-Skowrońska D, Michalak M, Dobrowolska G,  Sadowski J, Ludwików A. 2015. Arabidopsis ABA-activated kinase MAPKKK18 is regulated by protein phosphatase 2C ABI1 and the ubiquitin proteasome pathway. Plant and Cell Physiology, 56, 2351–2367.
Mukherjee D, Saha D, Acharya D, Mukherjee A, Chakraborty S, Ghosh T C. 2018. The role of introns in the conservation of the metabolic genes of Arabidopsis thaliana. Genomics, 110, 310–317.
Née G, Kramer K, Nakabayashi K, Yuan B, Xiang Y, Miatton E, Finkemeier I, Soppe W J J. 2017. DELAY OF GERMINATION1 requires PP2C phosphatases of the ABA signalling pathway to control seed dormancy. Nature Communications, 8, 72.
Nishimura N, Tsuchiya W, Moresco J J, Hayashi Y, Satoh K, Kaiwa N, Irisa T, Kinoshita T, Schroeder J T, YatesIII J R, Hirayama T, Yamazaki T. 2018. Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme. Nature Communications, 9, 2132.
Nishimura N, Yoshida T, Murayama M, Asami T, Shinozaki K, Hirayama T. 2004. Isolation and characterization of novel mutants affecting the abscisic acid sensitivity of Arabidopsis germination and seedling growth. Plant and Cell Physiology, 45, 1485–1499.
Park C J, Peng Y, Chen X W, Dardick C, Ruan D, Bart R, Canlas P E, Ronald P C. 2008. Rice XB15, a protein phosphatase 2C, negatively regulates cell death and XA21-mediated innate immunity. PLoS Biology, 6, e231.
Ren H, Park M Y, Spartz A K, Wong J H, Gray W M, 2018. A subset of plasma membrane-localized PP2C.D phosphatases negatively regulate SAUR-mediated cell expansion in Arabidopsis. PLoS Genetics, 14, e1007455.
Rodriguez P L, Benning G, Grill E. 1998. ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Letters, 421, 185–190.
Rouster J, Leah R, Mundy J, Cameron-Mills V. 1997. Identification of a methyl jasmonate-responsive region in the promoter of a lipoxygenase 1 gene expressed in barley grain. The Plant Journal, 11, 513–523.
Schweighofer A, Hirt H, Meskiene I. 2004. Plant PP2C phosphatases: Emerging functions in stress signaling. Trends in Plant Science, 9, 236–243.
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. 2007. PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. The Plant Cell, 19, 2213–2224.
Servet C, Benhamed M, Latrasse D, Kim W, Delarue M, Zhou D X. 2008. Characterization of a phosphatase 2C protein as an interacting partner of the histone acetyltransferase GCN5 in Arabidopsis. Biochimica et Biophysica Acta, 1779, 376–382.
Shen Q, Ho T H. 1995. Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-box and a novel cis-acting element. The Plant Cell, 7, 295–307.
Shiozaki K, Russell P. 1995. Counteractive roles of protein phosphatase 2C (PP2C) and a MAP kinase kinase homolog in the osmoregulation of fission yeast. The EMBO Journal, 14, 492–502.
Simpson S D, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2003. Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. The Plant Journal, 33, 259–270.
Singh A, Yadav A K, Kaur K, Sanyal S K, Jha S K, Fernandes J L, Sharma P, Tokas I, Pandey A, Sheng L, Pandey G K. 2018. A protein phosphatase 2C, AP2C1, interacts with and negatively regulates the function of CIPK9 under potassium-deficient conditions in Arabidopsis. Journal of Experimental Botany, 69, 4003–4015.
Song S K, Hofhuis H, Lee M M, Clark S E. 2008. Key divisions in the early Arabidopsis embryo require POL and PLL1 phosphatases to establish the root stem cell organizer and vascular axis. Developmental Cell, 15, 98–109.
Tovar-Mendez A, Miernyk J A, Hoyos E, Randall D D. 2014. A functional genomic analysis of Arabidopsis thaliana PP2C clade D. Protoplasma, 251, 265–271.
Xiao D, Cui Y, Xu F, Xu X, Gao G, Wang Y, Guo Z, Wang D, Wang N N. 2015. Senescence-suppressed protein phosphatase directly interacts with the cytoplasmic domain of senescence-associated receptor-like kinase and negatively regulates leaf senescence in Arabidopsis. Plant Physiology, 169, 1275–1291.
Xu G, Guo C, Shan H, Kong H. 2012. Divergence of duplicate genes in exon-intron structure. Proceedings of the National Academy of Sciences of the United States of America, 109, 1187–1192.
Xu X, Pan S, Cheng S, Zhang B, Mu D, Ni P, Zhang G, Yang S, Li R, Wang J, Orjeda G, Guzman F, Torres M, Lozano R, Ponce O, Martinez D, De la Cruz G, Chakrabarti S K, Patil V U, Skryabin K G, et al. 2011. Genome sequence and analysis of the tuber crop potato. Nature, 475, 189–195.
Xue T, Wang D, Zhang S, Ehlting J, Ni F, Jakab S, Zheng C, Zhong Y. 2008. Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis. BMC Genomics, 9, 550.
Yang S, Zhang X, Yue J X, Tian D, Chen J Q. 2008. Recent duplications dominate NBS-encoding gene expansion in two woody species. Molecular Genetics and Genomics, 280, 187–198.
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