Genome-wide identification and characterization of sweet orange (Citrus sinensis) aquaporin genes and their expression in two citrus cultivars differing in drought tolerance
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Aquaporins (AQPs), which belong to a highly conserved superfamily of major intrinsic proteins (MIPs), play key roles in regulation of movement of water and other small molecules across membranes. However, information concerning the AQP gene family in citrus is limited. Here, we conducted a genome-wide search for the homologs of AQPs in sweet orange and identified 34 full-length AQP genes (CsAQPs) that were located on all nine chromosomes. Phylogenetic analysis revealed that the CsAQPs could be classified into five subfamilies, including 11 plasma membrane intrinsic proteins (PIPs), nine tonoplast intrinsic proteins (TIPs), eight NOD26-like intrinsic proteins (NIPs), three small basic intrinsic proteins (SIPs), and three X intrinsic proteins (XIPs). Gene structure was generally conserved within each subfamily, with intron numbers ranging from zero to four. Functional prediction based on the analysis of the NPA motifs, aromatic/arginine (ar/R) selectivity filter, Froger’s positions, and specificity-determining positions (SDPs) revealed remarkable differences in substrate specificity among subfamilies. Furthermore, analysis of the transcription profile of CsAQP genes in the roots and leaves of drought-tolerant (HJ) and drought-sensitive (HH) cultivars under drought treatment revealed that most CsPIPs and CsTIPs were down-regulated in roots of both treated cultivars. In addition, the down-regulation of CsPIP1;2, CsTIP3;2, and CsNIP2;1 in roots and up-regulation of CsNIP1;1, CsNIP1;3, CsNIP4;1, and CsNIP5;1 in leaves revealed obvious differences between tolerant and sensitive cultivars during drought. Collectively, these findings provide valuable knowledge that furthers our understanding of the potential biological functions of AQP genes in drought tolerance of citrus.
KeywordsAquaporin Drought stress Gene expression Phylogenetic analysis Sweet orange
We thank LetPub (http://www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
This work was funded by the National Natural Science Foundation of China (Grant No.31460496, 31501811).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
This article does not contain any studies with animals performed by any of the authors.
- Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15:439–447. https://doi.org/10.1105/tpc.009225 CrossRefPubMedPubMedCentralGoogle Scholar
- Cohen D, Bogeat-Triboulot MB, Vialet-Chabrand S, Merret R, Courty PE, Moretti S, Bizet F, Guilliot A, Hummel I (2013) Developmental and environmental regulation of aquaporin gene expression across Populus species: divergence or redundancy? PLoS One 8:e55506. https://doi.org/10.1371/journal.pone.0055506 CrossRefPubMedPubMedCentralGoogle Scholar
- Deshmukh RK, Vivancos J, Guérin V, Sonah H, Labbé C, Belzile F, Be’langer RR (2013) Identification and functional characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice. Plant Mol Biol 83:303–317. https://doi.org/10.1007/s11103-013-0087-3 CrossRefPubMedGoogle Scholar
- Diehn TA, Pommerrenig B, Bernhardt N, Hartmann A, Bienert GP (2015) Genome-wide identification of aquaporin encoding genes in Brassica oleracea and their phylogenetic sequence comparison to Brassica crops and Arabidopsis. Front Plant Sci 6:166. https://doi.org/10.3389/fpls.2015.00 CrossRefPubMedPubMedCentralGoogle Scholar
- FAOSTAT http://www.fao.org/fao
- Gambetta GA, Fei J, Rost TL, Knipfer T, Matthews MA, Shackel KA, Walker MA, McElrone AJ (2013) Water uptake along the length of grapevine fine roots: developmental anatomy, tissue-specific aquaporin expression, and pathways of water transport. Plant Physiol 163:1254–1265. https://doi.org/10.1104/pp.113.221283 CrossRefPubMedPubMedCentralGoogle Scholar
- Gupta AB, Sankararamakrishnan R (2009) Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biol 9:134. https://doi.org/10.1186/1471-2229-9-134 CrossRefPubMedPubMedCentralGoogle Scholar
- Gu Z, Cavalcanti A, Chen F, Bouman P, Li W (2002) Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol 19:256–262. https://doi.org/10.1093/oxfordjournals.molbev.a004079 CrossRefPubMedGoogle Scholar
- Hu W, Hou XW, Huang C, Yan Y, Tie WW, Ding ZH, Wei YX, Liu JH, Mao HX, Lu ZW, Li MY, Xu BY, Jin ZQ (2015) Genome-wide identification and expression analyses of aquaporin gene family during development and abiotic stress in Banana. Int J Mol Sci 16:19728–19751. https://doi.org/10.3390/ijms160819728 CrossRefPubMedPubMedCentralGoogle Scholar
- Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjövall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126:1358–1369. https://doi.org/10.1104/pp.126.4.1358 CrossRefPubMedPubMedCentralGoogle Scholar
- Kalinina OV, Mironov AA, Gelfand MS, Rakhmaninova AB (2004) Automated selection of positions determining functional specificity of proteins by comparative analysis of orthologous groups in protein families. Protein Sci 13:443–456. https://doi.org/10.1110/ps.03191704 CrossRefPubMedPubMedCentralGoogle Scholar
- Kapilan R, Vaziri M, Zwiazek JJ (2018) Regulation of aquaporins in plants under stress. Biol Res 51(4). https://doi.org/10.1186/s40659-018-0152-0
- Martins CDPS, Pedrosa AM, Du DL, Gonçalves LPYQB, Gmitter FG, Gilberto F, Costa C (2015) Genome-wide characterization and expression analysis of major intrinsic proteins during abiotic and biotic stresses in sweet orange (Citrus sinensis L. Osb.). PLoS One 10:e0138786. https://doi.org/10.1371/journal.pone.0138786 CrossRefGoogle Scholar
- Perrone I, Gambino G, Chitarra W, Vitali M, Pagliarani C, Riccomagno N, Balestrini F, Kaldenhoff R, Uehlein N, Gribaudo I, Schubert A, Lovisolo C (2012) The grapevine root-specific aquaporin VvPIP2;4N controls root hydraulic conductance and leaf gas exchange under well-watered conditions but not under water stress. Plant Physiol 160:965–977. https://doi.org/10.1104/pp.112.203455 CrossRefPubMedPubMedCentralGoogle Scholar
- Sade N, Vinocur B, Diber A, Shatil A, Ronen G, Nissan H, Wallach R, Karchi H, Moshelion M (2009) Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion? New Phytol 181:651–661. https://doi.org/10.1111/j.1469-8137.2008.02689.x CrossRefPubMedGoogle Scholar
- Tao P, Zhong XM, Li BY, Wang WH, Yue ZC, Lei JL, Guo WL, Huang XY (2014) Genome-wide identification and characterization of aquaporin genes (AQPs) in Chinese cabbage (Brassica rapa ssp. pekinensis). Mol Genet Genomics 289:1131–1145. https://doi.org/10.1007/s00438-014-0874-9 CrossRefPubMedGoogle Scholar
- Wang X, Cai H, Li Y, Zhu YM, Ji W, Bai X, Zhu D, Sun XL (2015) Ectopic overexpression of a novel Glycine soja, stress-induced plasma membrane intrinsic protein increases sensitivity to salt and dehydration in transgenic Arabidopsis thaliana plants. J Plant Res 128:103–113. https://doi.org/10.1007/s10265-014-0674-7 CrossRefPubMedGoogle Scholar
- Wang C, Wang LQ, Yang CP, Wang YC (2017) Identification, phylogeny, and transcript profiling of aquaporin genes in response to abiotic stress in Tamarix hispida. Tree Genet Genomes 13(81). https://doi.org/10.1007/s11295-017-1163-7
- Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao WB, Hao BH, Lyon MP, Chen J, Gao S, Xing F, Lan H, Chang JW, Ge X, Lei Y, Hu Q, Miao Y, Wang L, Xiao S, Biswas MK, Zeng W, Guo F, Cao H, Yang X, Xu XW, Cheng YJ, Xu J, Liu JH, Luo OJ, Tang Z, Guo WW, Kuang H, Zhang HY, Roose ML, Nagarajan N, Deng XX, Ruan Y (2012) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66. https://doi.org/10.1038/ng.2472 CrossRefPubMedGoogle Scholar
- Yuan D, Li W, Hua YP, King GJ, Xu FS, Shi L (2017) Genome-wide identification and characterization of the aquaporin gene family and transcriptional responses to boron deficiency in Brassica napus. Front Plant Sci 8(1336). https://doi.org/10.3389/fpls.2017.01336
- Zhang DY, Ali Z, Wang CB, Xu L, Yi JX, Xu ZL, Liu XQ, He XL, Huang HY, Khan IA, Trethowan RM, Ma HX (2013) Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.). PLoS One 8. https://doi.org/10.1371/journal.pone.0056312 CrossRefGoogle Scholar
- Zou Z, Gong J, An F, Xie GS, Wang JK, Mo YY, Yang LF (2015) Genome-wide identification of rubber tree (Hevea brasiliensis Muell. Arg.) aquaporin genes and their response to ethephon stimulation in the laticifer, a rubber-producing tissue. BMC Genomics 16(1):–18. https://doi.org/10.1186/s12864-0152152-6
- Zou Z, Yang LF, Gong J, Mo YY, Wang JK, Cao JH, An F, Xie GS (2016) Genome-wide identification of Jatropha curcas aquaporin genes and the comparative analysis provides insights into the gene family expansion and evolution in Hevea brasiliensis. Front Plant Sci 7(395). https://doi.org/10.3389/fpls.2016.00395