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Phylogenetic and ion-response analyses reveal a relationship between gene expansion and functional divergence in the Ca2+/cation antiporter family in Angiosperms

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Plant CaCA superfamily genes with higher tendency to retain after WGD are more gene expression and function differentiated in ion-response.

Abstract

Plants and animals face different environmental stresses but share conserved Ca2+ signaling pathways, such as Ca2+/Cation transport. The Ca2+/cation antiporters superfamily (CaCAs) is an ancient and widespread family of ion-coupled cation transporters found in all kingdoms of life. We analyzed the molecular evolution progress of the family through comparative genomics and phylogenetics of CaCAs genes from plants and animals, grouping these genes into several families and clades, and identified multiple gene duplication retention events, particularly in the CAX (H+/cation exchanger), CCX (cation/Ca2+ exchanger), and NCL (Na+/Ca2+ exchanger-like) families. The tendency of duplication retention differs between families and gene clades. The gene duplication events were probably the result of whole-genome duplication (WGD) in plants and might have led to functional divergence. Tissue and ion-response expression analyses revealed that CaCAs genes with more highly differentiated expression patterns are more likely to be retained as duplicates than those with more conserved expression profiles. Phenotype of Arabidopsis thaliana mutants showed that loss of genes with a greater tendency to be retained after duplication resulted in more severe growth deficiency. CaCAs genes in salt-tolerant species tended to inherit the expression characteristics of their most recent common ancestral genes, with conservative ion-response expression. This study indicates a possible evolutionary scheme for cation transport and illustrates distinct fates and a mechanism for the evolution of gene duplicates. The increased copy numbers of genes and divergences in expression might have contributed to the divergent functions of CaCAs protein, allowing plants to cope with environmental stresses and adapt to a larger number of ecological niches.

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References

  • Adams P, Thomas JC, Vernon DM, Bohnert HJ, Jensen RG (1992) Distinct cellular and organismic responses to salt stress. Plant Cell Physiol 33:1215–1223

    CAS  Google Scholar 

  • Akhilesh KY, Alka S, Saroj KJ, Poonam K, Amita P, Girdhar KP (2015) A rice tonoplastic calcium exchanger, OsCCX2 mediates Ca2+/cation transport in yeast. Sci Rep 5:17117

    Article  CAS  Google Scholar 

  • Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258

    Article  CAS  PubMed  Google Scholar 

  • Ben-Amotz A, Avron M (1990) The biotechnology of cultivating the halotolerant alga Dunaliella. Trends Biotechnol 8:121–126

    Article  CAS  Google Scholar 

  • Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signaling: dynamics, homeostasis, and remodeling. Nat Rev Mol Cell Biol 4:517–529

    Article  CAS  PubMed  Google Scholar 

  • Blaustein MP, Lederer WJ (1999) Sodium/calcium exchange: its physiological implications. Physiol Rev 79:763–854

    Article  CAS  PubMed  Google Scholar 

  • Bonza MC, Loro G, Behera S, Wong A, Kudla J, Costa A (2013) Analyses of Ca2+ accumulation and dynamics in the endoplasmic reticulum of Arabidopsis root cells using a genetically encoded Cameleon sensor. Plant Physiol 163:1230–1241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brenchley R, Spannagl M, Pfeifer M, Barker GL, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo MC, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KF, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491:705–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai X, Clapham DE (2012) Ancestral Ca2+ signaling machinery in early animal and fungal evolution. Mol Biol Evol 29:91–100

    Article  PubMed  CAS  Google Scholar 

  • Cai XJ, Lytton J (2004) The cation/Ca2+ exchanger superfamily: phylogenetic analysis and structural implications. Mol Biol Evol 21:1692–1703

    Article  CAS  PubMed  Google Scholar 

  • Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cheng NH, Pittman JK, Barkla BJ, Shigaki T, Hirschi KD (2003) The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 15:347–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng NH, Pittman JK, Zhou JK, Hirschi KD (2004) The protein kinase SOS2 activates the Arabidopsis H (+)/Ca (2+) antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem 279:2922–2926

    Article  CAS  PubMed  Google Scholar 

  • Cheng NH, Pittman JK, Shigaki T, Lachmansingh J, LeClere S, Lahner B, Salt DE, Hirschi KD (2005) Functional association of Arabidopsis CAX1 and CAX3 are required for normal growth and ion homeostasis. Plant Physiol 138:2048–2060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi WG, Toyota M, Kim SH, Hilleary R, Gilroy S (2014) Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci USA 111:6497–6502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi WG, Hilleary R, Swanson SJ, Kim S-H, Gilroy S (2016) Rapid, long-distance electrical and calcium signaling in plants. Annu Rev Plant Biol 67:287–307

    Article  CAS  PubMed  Google Scholar 

  • Conn SJ, Gilliham M, Athman A, Schreiber AW, Baumann U, Moller I, Cheng NH, Stancombe MA, Hirschi KD, Webb AA, Burton R, Kaiser BN, Tyerman SD, Leigh RA (2011) Cell-specific vacuolar calcium storage mediated by CAX1 regulates apoplastic calcium concentration, gas exchange, and plant productivity in Arabidopsis. Plant Cell 23:240–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corso M, Doccula FG, de Melo JRF, Costa A, Verbruggen N (2018) Endoplasmic reticulum-localized CCX2 is required for osmotolerance by regulating ER and cytosolic Ca2+ dynamics in Arabidopsis. Proc Nati Acad Sci USA 115:3966–3971

    Article  CAS  Google Scholar 

  • Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, Doyle JJ, Soltis PS, Carlson JE, Arumuganathan K, Barakat A, Albert VA, Ma H, dePamphilis CW (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16:738–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Derelle E, Ferraz C, Rombauts S, Rouzé P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynié S, Cooke R, Saeys Y, Wuyts J, Jabbari K, Bowler C, Panaud O, Piégu B, Ball SG, Ral JP, Bouget FY, Piganeau G, De Baets B, Picard A, Delseny M, Demaille J, Van de Peer Y, Moreau H (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103:11647–11652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620

    Article  CAS  PubMed  Google Scholar 

  • Edel KH, Marchadier E, Brownlee C, Kudla J, Hetherington AM (2017) The evolution of calcium-based signaling in plants. Curr Biol 27:R667–R679

    Article  CAS  PubMed  Google Scholar 

  • Edmond C, Shigaki T, Ewert S, Nelson MD, Connorton JM, Chalova V, Noordally Z, Pittman JK (2009) Comparative analysis of CAX2-like cation transporters indicates functional and regulatory diversity. Biochem J 418:145–154

    Article  CAS  PubMed  Google Scholar 

  • Emery L, Whelan S, Hirschi KD, Pittman JK (2012) Protein phylogenetic analysis of Ca2+/cation antiporters and insights into their evolution in plants. Front Plant Sci 3:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:29–37

    Article  CAS  Google Scholar 

  • Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285

    Article  CAS  PubMed  Google Scholar 

  • Fox TC, Guerinot ML (1998) Molecular biology of cation transport in plants. Annu Rev Plant Biol 49:669–696

    Article  CAS  Google Scholar 

  • Gaash R, Elazar M, Mizrahi K, Avramov-Mor M, Berezin I, Shaul O (2013) Phylogeny and a structural model of plant MHX transporters. BMC Plant Biol 13:75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han N, Lan WJ, He X, Shao Q, Wang B-S, Zhao X-J (2012) Expression of a Suaeda salsa vacuolar H+/Ca2+ transporter gene in Arabidopsis contributes to physiological changes in salinity. Plant Mol Biol Rep 30:470–477

    Article  CAS  Google Scholar 

  • Harris E (1989) The chlamydomonas sourcebook. Academic Press, San Diego, pp 25–63

    Book  Google Scholar 

  • Hirschi K (2001) Vacuolar H+/Ca2+ transport: who’s directing the traffic? Trends Plant Sci 6:100–104

    Article  CAS  PubMed  Google Scholar 

  • Hirschi KD (1999) Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11:2113–2122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang CH, Sun R, Hu Y, Zeng L, Zhang N, Cai L, Zhang Q, Koch MA, Al-Shehbaz I, Edger PP, Pires JC, Tan DY, Zhong Y, Ma H (2016a) Resolution of Brassicaceae phylogeny using nuclear genes uncovers nested radiations and supports convergent morphological evolution. Mol Biol Evol 33:394–412

    Article  CAS  PubMed  Google Scholar 

  • Huang CH, Zhang C, Liu M, Hu Y, Gao T, Qi J, Ma H (2016b) Multiple polyploidization events across Asteraceae with two nested events in the early history revealed by nuclear phylogenomics. Mol Biol Evol 33:2820–2835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivey DM, Guffanti AA, Zemsky J, Pinner E, Karpel R, Padan E, Schuldiner S, Krulwich TA (1993) Cloning and characterization of a putative Ca2+/H+ antiporter gene from Escherichia coli upon functional complementation of Na+/H+ antiporter-deficient strains by the overexpressed gene. J Biol Chem 268:11296–11303

    Article  CAS  PubMed  Google Scholar 

  • Iyengar ERR, Reddy MP (1996) Photosynthesis in highly salt-tolerant plants. In: Pesserkali M (ed) Handbook of photosynthesis. Marshal Dekar, Baten Rose, pp 897–909

    Google Scholar 

  • Jiang WT, Wang Q-X, Wu S-X (2007) Primary study of the photosynthetic characteristics of Chlamydomonas reinhardtii strain 849 under salty stress. Bull Bot Res 3:284–288

    Google Scholar 

  • Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang HY, Soltis PS, Soltis DE, Clifton SW, Schlarbaum SE, Schuster SC, Ma H, Leebens-Mack J, de Pamphilis CW (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Leebens-Mack J, Ayyampalayam S, Bowers JE, McKain MR, McNeal J, Rolf M, Ruzicka DR, Wafula E, Wickett NJ, Wu X, Zhang Y, Wang J, Zhang Y, Carpenter EJ, Deyholos MK, Kutchan TM, Chanderbali AS, Soltis PS, Stevenson DW, McCombie R, Pires JC, Wong GK, Soltis DE, Depamphilis CW (2012) A genome triplication associated with early diversification of the core eudicots. Genome Biol 13:R3

    Article  PubMed  PubMed Central  Google Scholar 

  • Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamiya T, Akahori T, Maeshima M (2005) Expression profile of the genes for rice cation/H+ exchanger family and functional analysis in yeast. Plant Cell Physiol 46:1735–1740

    Article  CAS  PubMed  Google Scholar 

  • Katoh K, Rozewicki J, Yamada KD (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform bbx108:1–7

    Google Scholar 

  • Khananshvili D (2013) The SLC8 gene family of sodium-calcium exchangers (NCX)-structure, function, and regulation in health and disease. Mol Aspects Med 34:220–235

    Article  CAS  PubMed  Google Scholar 

  • Khananshvili D (2014) Sodium-calcium exchangers (NCX): Molecular hallmarks underlying the tissue-specific and systemic functions. Eur J Physiol 466:43–60

    Article  CAS  Google Scholar 

  • Lei G-P, Qiao D-R, Bai L-H, Xu H, Cao Y (2008) Isolation and characterization of a mitogen-activated protein kinase gene in the halotolerant alga Dunaliella salina. J Appl Phycol 20:13–17

    Article  CAS  Google Scholar 

  • Li W-W, Zhou M-Q, Zheng Y, Lin P, Yao X-H, Lin J (2017) Characterization of CbCAX51, a cold responsive Ca2+/H+ exchanger from Capsella bursa-pastoris modulating cold Tolerance in plants. Int J Agric Biol 19:817–824

    Article  CAS  Google Scholar 

  • Li Y, Sun W, Liu F, cheng J, Zhang X, Zhang H, Zhao J (2019) Methods for grafting Arabidopsis thaliana and Eutrema salsugineum. Plant Methods 15:93

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li Z-P, Wang X-L, Chen J-Y, Gao J, Zhou X, Kuai B-K (2016) CCX1, a putative Cation/Ca2+ exchanger, participates in regulation of reactive oxygen species homeostasis and leaf senescence. Plant Cell Physiol 57:2611–2619

    Article  CAS  PubMed  Google Scholar 

  • Luo GZ, Wang HW, Huang J, Tian AG, Wang YJ, Zhang JS, Chen SY (2005) A putative plasma membrane cation/proton antiporter from soybean confers salt tolerance in Arabidopsis. Plant Mol Biol 59:809–820

    Article  CAS  PubMed  Google Scholar 

  • Lytton J (2007) Na+/Ca2+ exchangers: three mammalian gene families control Ca2+ transport. Biochem J 406:365–382

    Article  CAS  PubMed  Google Scholar 

  • Magadum S, Banerjee U, Murugan P, Gangapur D, Ravikesavan R (2013) Gene duplication as a major force in evolution. J Genet 92:155–161

    Article  PubMed  Google Scholar 

  • Manohar M, Shigaki T, Hirschi KD (2011) Plant cation/H+ exchangers (CAXs): biological functions and genetic manipulations. Plant Biol 13:561–569

    Article  CAS  PubMed  Google Scholar 

  • Manohar M, Shigaki T, Mei H, Park S, Marshall J, Aguilar J, Hirschi KD (2011) Characterization of Arabidopsis Ca2+/H+ exchanger CAX3. Biochemistry 50:6189–6195

    Article  CAS  PubMed  Google Scholar 

  • Marty F (1999) Plant vacuoles. Plant Cell 11:587–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mei H, Zhao J, Pittman JK, Lachmansingh J, Park SH, Hirschi KD (2007) In planta regulation of the Arabidopsis Ca (2+)/H (+) antiporter CAX1. J Exp Bot 58:3419–3427

    Article  CAS  PubMed  Google Scholar 

  • Mei H, Cheng N-H, Zhao J, Park SH, Escareno RA, Pittman JK, Hirschi KD (2009) Root development under metal stress in Arabidopsis thaliana requires the H+/cation antiporter CAX4. New Phytol 183:95–105

    Article  CAS  PubMed  Google Scholar 

  • Morris J, Tian H, Sunghun P (2008) AtCCX3 is an Arabidopsis endomembrane H+-dependent K+ transporter. Plant Physiol 148:1474–1486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murat F, Peer YV, Salse J (2012) Decoding plant and animal genome plasticity from differential paleo-evolutionary patterns and processes. Genome Biol Evolut 4:917–928

    Article  CAS  Google Scholar 

  • Nakamura Y, Kaneko T, Sato S, Ikeuchi M, Katoh H, Sasamoto S, Watanabe A, Iriguchi M, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Nakazaki N, Shinpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S (2002) Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res 31:123–130

    Article  Google Scholar 

  • Norris V, Grant S, Freestone P, Canvin J, Sheikh FN, Toth I, Trinei M, Modha K, Norman RI (1996) Calcium signaling in bacteria. J Bacteriol 178:3677–3682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer, New York

    Book  Google Scholar 

  • Panchy N, Lehti-Shiu M, Shiu SH (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pellicer J, Fay MF, Leitch IJ (2010) The largest eukaryotic genome of them all? Bot J Linn Soc 164:10–15

    Article  Google Scholar 

  • Philipson KD, Nicoll DA (2000) Sodium-calcium exchange: a molecular perspective. Annu Rev Physiol 62:111–133

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK, Hirschi KD (2016a) CAX-ing a wide net: Cation/H (+) transporters in metal remediation and abiotic stress signaling. Plant Biol 18:741–749

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK, Hirschi KD (2016b) Phylogenetic analysis and protein structure modelling identifies distinct Ca (2+)/cation antiporters and conservation of gene family structure within Arabidopsis and rice species. Rice 9:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Pittman JK, Shigaki T, Hirschi KD (2005) Evidence of differential pH regulation of the Arabidopsis vacuolar Ca2+/H+ antiporters CAX1 and CAX2. FEBS Lett 579:2648–2656

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK, Shigaki T, Marshall JL, Morris JL, Cheng NH, Hirschi KD (2004) Functional and regulatory analysis of the Arabidopsis thaliana CAX2 cation transporter. Plant Mol Biol 56:959–971

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK, Edmond C, Sunderland PA, Bray CM (2009) A cation-regulated and proton gradient- dependent cation transporter from Chlamydomonas reinhardtii has a role in calcium and sodium homeostasis. J Biol Chem 284:525–533

    Article  CAS  PubMed  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2009) Fasttree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Punshon T, Hirschi K, Yang J, Lanzirotti A, Lai B, Guerinot ML (2012) The role of CAX1 and CAX3 in elemental distribution and abundance in Arabidopsis seed. Plant Physiol 158:352–362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy MP, Sanish S, Iyengar ERR (1992) Photosynthetic studies and compartmentation of ions in different tissues of Salicornia brachiata Roxb. under saline conditions. Photosynthetica 26:173–179

    CAS  Google Scholar 

  • Ren R, Wang H, Guo C, Zhang N, Zeng L, Chen Y, Ma H, Qi J (2018) Widespread whole genome duplications contribute to genome complexity and species diversity in angiosperms. Mol Plant 11:414–428

    Article  CAS  PubMed  Google Scholar 

  • Rivero L, Scholl R, Holomuzki N, Crist D, Grotewold E, Brkljacic J (2014) Handling Arabidopsis plants: growth, preservation of seeds, transformation, and genetic crosses. Methods Mol Biol 1062:3–25

    Article  PubMed  CAS  Google Scholar 

  • Rosen BP (1987) Bacterial calcium transport. Biochem Biophys Acta 906:101–110

    CAS  PubMed  Google Scholar 

  • Saier MH, Eng BH, Fard S, Garg J, Haggerty DA, Hutchinson WJ, Jack DL, Lai E-C, Liu H-J, Nusinew DP, Omar AM, Pao S-S, Paulsen IT, Quan JA, Sliwinski M, Tseng TT, Wachi S, Young G-B (1999) Phylogenetic characterization of novel transport protein families revealed by genome analyses. Biochim Biophys Acta (BBA) Rev Biomembr 1422:1–56

    Article  CAS  Google Scholar 

  • Schmutz J, Steven B, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song QJ, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  CAS  PubMed  Google Scholar 

  • Shaul O, Hilgemann DW, de-Almeida-Engler J, Van Montagu M, Inze D, Galili G (1999) Cloning and characterization of a novel Mg2+/H+ exchanger. EMBO J 18:3973–3980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigaki T, Hirschi KD (2006) Diverse functions and molecular properties emerging for CAX cation/H+ exchangers in plants. Plant Biol 8:419–429

    Article  CAS  PubMed  Google Scholar 

  • Shigaki T, Pittman JK, Hirschi KD (2003) Manganese specificity determinants in the Arabidopsis metal/H+ antiporter CAX2. J Biol Chem 278:6610–6617

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Kanwar P, Yadav AK, Mishra M, Jha SK, Baranwal V, Pandey A, Kapoor S, Tyagi AK, Pandey GK (2014) Genome-wide expressional and functional analysis of calcium transport elements during abiotic stress and development in rice. FEBS J 281:894–915

    Article  CAS  PubMed  Google Scholar 

  • Singh AK, Kumar R, Tripathi AK, Gupta BK, Pareek A, Pareek-Singla SL (2015) Genome-wide investigation and expression analysis of sodium/calcium exchanger gene family in rice and Arabidopsis. Rice 8:21

    Article  PubMed Central  Google Scholar 

  • Smith JDL, Bickham JW, Gregory TR (2013) Patterns of genome size diversity in bats (order Chiroptera). Genome 56:457–472

    Article  PubMed  Google Scholar 

  • Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava RK, Pandey P, Rajpoot R, Rani A, Gautam A, Dubey RS (2015) Exogenous application of calcium and silica alleviates cadmium toxicity by suppressing oxidative damage in rice seedlings. Protoplasma 252:959–975

    Article  CAS  PubMed  Google Scholar 

  • Taneja M, Tyagi S, Sharma S, Upadhyay SK (2016) Ca2+/Cation Antiporters (CaCA): identification, characterization and expression profiling in bread wheat (Triticum aestivum L.). Front Plant Sci 7:1775

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanneste K, Baele G, Maere S, Van de Peer Y (2014) Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the cretaceous-paleogene boundary. Genome Res 24:1334–1347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waditee R, Hossain GS, Tanaka Y, Nakamura T, Shikata M, Takano J, Takabe T, Takabe T (2004) Isolation and functional characterization of Ca2+/H+ antiporters from cyanobacteria. J Biol Chem 279:4330–4338

    Article  CAS  PubMed  Google Scholar 

  • Wang BS, Luttge U, Ratajczak R (2001) Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. J Exp Bot 52:2355–2365

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Li Z, Wei J, Zhao Z, Sun D, Cui S (2012) A Na+/Ca2+ exchanger-like protein (AtNCL) involved in salt stress in Arabidopsis. J Biol Chem 287:44062–44070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Y-C, Rasmussen MD, Bansal MS, Kellis M (2013) TreeFix: statistically informed gene tree error correction using species trees. Syst Biol 62:110–120

    Article  PubMed  Google Scholar 

  • Xiang Y, Huang CH, Hu Y, Wen J, Li S, Yi T, Chen H, Xiang J, Ma H (2017) Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication. Mol Biol Evol 34:262–281

    CAS  PubMed  Google Scholar 

  • Yamada N, Theerawitaya C, Cha-um S, Kirdmanee C, Takabe T (2014) Expression and functional analysis of putative vacuolar Ca2+-transporters (CAXs and ACAs) in roots of salt tolerant and sensitive rice cultivars. Protoplasma 251:1067–1075

    Article  CAS  PubMed  Google Scholar 

  • Zeng L, Zhang Q, Sun R, Kong H, Zhang N, Ma H (2014) Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times. Nat Commun 5:4956

    Article  CAS  PubMed  Google Scholar 

  • Zeng L, Zhang N, Zhang Q, Endress PK, Huang J, Ma H (2017) Resolution of deep eudicot phylogeny and their temporal diversification using nuclear genes from transcriptomic and genomic datasets. New Phytol 214:1338–1354

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Landback P, Gschwend AR, Shen B, Long M (2015) New genes drive the evolution of gene interaction networks in the human and mouse genomes. Genome Biol 16:202

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang F, Cui F, Zhang L, Wen X, Luo X, Zhou Y, Li X, Wan Y, Zheng J, Xie J-K (2014) Development and identification of an introgression line with strong drought resistance at seedling stage derived from Oryza sativa L. mating with Oryza rufipogon Griff. Euphytica 200:1–7

    Article  CAS  Google Scholar 

  • Zhang X, Zhang M, Takano T, Liu S (2011) Characterization of an AtCCX5 gene from Arabidopsis thaliana that involves in high-affinity K+ uptake and Na+ transport in yeast. Biochem Biophys Res Commun 414:96–100

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Barkla BJ, Marshall J, Pittman JK, Hirschi KD (2008) The Arabidopsis cax3 mutants display altered salt tolerance, pH sensitivity and reduced plasma membrane H+-ATPase activity. Planta 227:659–969

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Shigaki T, Mei H, Guo Y-Q, Cheng N-H, Hirschi KD (2009) Interaction between Arabidopsis Ca2+/H+ exchangers CAX1 and CAX3. J Biol Chem 284:4605–4615

    Article  CAS  PubMed  Google Scholar 

  • Zhu J-K (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  CAS  PubMed  Google Scholar 

  • Zou C, LehtiShiu MD, Thomashow M, Shiu SH (2009) Evolution of stress-regulated gene expression in duplicate genes of Arabidopsis thaliana. PLoS Genet 5:e1000581

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

This work was supported by grants from National Natural Science Foundation of China (31170287 to J.L.) and Science and Technology Research Program of Shanghai (19DZ2282100 to J.L.).

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Authors and Affiliations

  1. State Key Laboratory of Genetic Engineering, Institute of Plant Biology, Shanghai Engineering Research Center of Industrial Microorganisms, School of Life Sciences, Fudan University, Shanghai, 200433, People’s Republic of China

    Ye Zheng, Lin-Bo Wang, Shu-Feng Sun, Shi-Ying Liu, Ming-Jia Liu & Juan Lin

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  1. Ye Zheng
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  2. Lin-Bo Wang
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  3. Shu-Feng Sun
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  4. Shi-Ying Liu
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  5. Ming-Jia Liu
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  6. Juan Lin
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Contributions

JL designed the study. YZ and LW carried out evolutionary analysis. YZ and SS carried out expression and ion response analysis. YZ, SL and ML prepared the plant materials. YZ drafted the manuscript. JL, YZ, SS and LW revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Juan Lin.

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Zheng, Y., Wang, LB., Sun, SF. et al. Phylogenetic and ion-response analyses reveal a relationship between gene expansion and functional divergence in the Ca2+/cation antiporter family in Angiosperms. Plant Mol Biol 105, 303–320 (2021). https://doi.org/10.1007/s11103-020-01088-7

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