Genome-wide analysis of MATE transporters and response to metal stress in Cajanus cajan

References

• Amalraj T, Ignacimuthu S. 1998. Hypoglycemic activity of Cajanus cajan (seeds) in mice. Indian J Exp Biol. 36:1032–1033.
   PubMedGoogle Scholar
• Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, de Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E, et al. 2012. ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res. 40:W597–W603. doi: 10.1093/nar/gks400
   PubMed Web of Science ®Google Scholar
• Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37:W202–W208. doi: 10.1093/nar/gkp335
   PubMed Web of Science ®Google Scholar
• Borges-Walmsley MI, McKeegan KS, Walmsley AR. 2003. Structure and function of efflux pumps that confer resistance to drugs. Biochem J. 376:313–338. doi: 10.1042/bj20020957
   PubMed Web of Science ®Google Scholar
• Brown MH, Paulsen IT, Skurray RA. 1999. The multidrug efflux protein NorM is a prototype of a new family of transporters. Mol Microbiol. 31:394–395. doi: 10.1046/j.1365-2958.1999.01162.x
   PubMed Web of Science ®Google Scholar
• Burns MJ, Edwards KJ, Newbury HJ, Ford-Lloyd BV, Baggott CD. 2001. Development of simple sequence repeat (SSR) markers for the assessment of gene flow and genetic diversity in pigeonpea (Cajanus cajan). Mol Ecol Notes. 1:283–285. doi: 10.1046/j.1471-8278.2001.00109.x
   Google Scholar
• Chai YR, Lei B, Huang HL, Li JN, Yin JM, Tang ZL, Wang R, Chen L. 2009. TRANSPARENT TESTA 12 genes from Brassica napus and parental species: cloning, evolution, and differential involvement in yellow seed trait. Mol Genet Genomics. 281:109–123. doi: 10.1007/s00438-008-0399-1
   PubMed Web of Science ®Google Scholar
• Chang HF, Wang SL, Yeh KC. 2017. Effect of Gallium exposure in Arabidopsis thaliana is similar to aluminum stress. Environ Sci Technol. 51:1241–1248. doi: 10.1021/acs.est.6b05760
   PubMed Web of Science ®Google Scholar
• Charlier JB, Polese C, Nouet C, Carnol M, Bosman B, Kramer U, Motte P, Hanikenne M. 2015. Zinc triggers a complex transcriptional and post-transcriptional regulation of the metal homeostasis gene FRD3 in Arabidopsis relatives. J Exp Bot. 66:3865–3878. doi: 10.1093/jxb/erv188
   PubMed Web of Science ®Google Scholar
• Debeaujon I, Peeters AJ, Leon-Kloosterziel KM, Koornneef M. 2001. The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell. 13:853–872. doi: 10.1105/tpc.13.4.853
   PubMed Web of Science ®Google Scholar
• Diener AC, Gaxiola RA, Fink GR. 2001. Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins. Plant Cell. 13:1625–1638. doi: 10.1105/TPC.010035
   PubMed Web of Science ®Google Scholar
• Divya C, Natasha S, Kathryn AV, David FG, Deborah A. 2001. Physiological and molecular characterization of aluminum resistance in Medicago truncatula. BMC Plant Biol. 8:89.
   Google Scholar
• Doshi R, McGrath AP, Pineros M, Szewczyk P, Garza DM, Kochian LV, Chang G. 2017. Functional characterization and discovery of modulators of SbMATE, the agronomically important aluminium tolerance transporter from Sorghum bicolor. Sci Rep. 7:17996. doi: 10.1038/s41598-017-18146-8
   PubMed Web of Science ®Google Scholar
• Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, et al. 2014. Pfam: the protein families database. Nucleic Acids Res. 42:D222–D230. doi: 10.1093/nar/gkt1223
   PubMed Web of Science ®Google Scholar
• Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF. 2007. An aluminum-activated citrate transporter in barley. Plant Cell Physiol. 48:1081–1091. doi: 10.1093/pcp/pcm091
   PubMed Web of Science ®Google Scholar
• Garcia-Oliveira AL, Martins-Lopes P, Tolra R, Poschenrieder C, Tarquis M, Guedes-Pinto H, Benito C. 2014. Molecular characterization of the citrate transporter gene TaMATE1 and expression analysis of upstream genes involved in organic acid transport under Al stress in bread wheat (Triticum aestivum). Physiol Plant. 152:441–452. doi: 10.1111/ppl.12179
   PubMed Web of Science ®Google Scholar
• Gomez C, Conejero G, Torregrosa L, Cheynier V, Terrier N, Ageorges A. 2011. In vivo grapevine anthocyanin transport involves vesicle-mediated trafficking and the contribution of anthoMATE transporters and GST. Plant J. 67:960–970. doi: 10.1111/j.1365-313X.2011.04648.x
   PubMed Web of Science ®Google Scholar
• Gomez C, Terrier N, Torregrosa L, Vialet S, Fournier-Level A, Verries C, Souquet JM, Mazauric JP, Klein M, Cheynier V, et al. 2009. Grapevine MATE-type proteins act as vacuolar H+-dependent acylated anthocyanin transporters. Plant Physiol. 150:402–415. doi: 10.1104/pp.109.135624
   PubMed Web of Science ®Google Scholar
• Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, et al. 2012. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40:D1178–D1186. doi: 10.1093/nar/gkr944
   PubMed Web of Science ®Google Scholar
• Grover JK, Yadav S, Vats V. 2002. Medicinal plants of India with anti-diabetic potential. J Ethnopharmacol. 81:81–100. doi: 10.1016/S0378-8741(02)00059-4
   PubMed Web of Science ®Google Scholar
• Guo X, Wang Y, Lu H, Cai X, Wang X, Zhou Z, Wang C, Wang Y, Zhang Z, Wang K, et al. 2017. Genome-wide characterization and expression analysis of the aldehyde dehydrogenase (ALDH) gene superfamily under abiotic stresses in cotton. Gene. 628:230–245. doi: 10.1016/j.gene.2017.07.034
   PubMed Web of Science ®Google Scholar
• Jacquemin J, Ammiraju JS, Haberer G, Billheimer DD, Yu Y, Liu LC, Rivera LF, Mayer K, Chen M, Wing RA. 2014. Fifteen million years of evolution in the Oryza genus shows extensive gene family expansion. Mol Plant. 7:642–656. doi: 10.1093/mp/sst149
   PubMed Web of Science ®Google Scholar
• Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ. 2015. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc. 10:845–858. doi: 10.1038/nprot.2015.053
   PubMed Web of Science ®Google Scholar
• Khan AA, McNeilly T, Collins JC. 2000. Accumulation of amino acids, proline, and carbohydrates in response to aluminum and manganese stress in maize. J Plant Nutr. 23:1303–1314. doi: 10.1080/01904160009382101
   Web of Science ®Google Scholar
• Li C, Zhao Q, Gao T, Wang H, Zhang Z, Liang B, Wei Z, Liu C, Ma F. 2018. The mitigation effects of exogenous melatonin on replant disease in apple. J Pineal Res. 65:e12523. doi: 10.1111/jpi.12523
   PubMed Web of Science ®Google Scholar
• Li GZ, Wang ZQ, Yokosho K, Ding B, Fan W, Gong QQ, Li GX, Wu YR, Yang JL, Ma JF, et al. 2018. Transcription factor WRKY22 promotes aluminum tolerance via activation of OsFRDL4 expression and enhancement of citrate secretion in rice (Oryza sativa). New Phytol. 219:149–162. doi: 10.1111/nph.15143
   PubMed Web of Science ®Google Scholar
• Li L, He Z, Pandey GK, Tsuchiya T, Luan S. 2002. Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. J Biol Chem. 277:5360–5368. doi: 10.1074/jbc.M108777200
   PubMed Web of Science ®Google Scholar
• Li N, Meng H, Xing H, Liang L, Zhao X, Luo K. 2017. Genome-wide analysis of MATE transporters and molecular characterization of aluminum resistance in populus. J Exp Bot. 68:5669–5683. doi: 10.1093/jxb/erx370
   PubMed Web of Science ®Google Scholar
• Li R, Li J, Li S, Qin G, Novak O, Pencik A, Ljung K, Aoyama T, Liu J, Murphy A, et al. 2014. ADP1 affects plant architecture by regulating local auxin biosynthesis. PLoS Genet. 10:e1003954. doi: 10.1371/journal.pgen.1003954
   PubMed Web of Science ®Google Scholar
• Liang BW, Ma CQ, Zhang ZJ, Wei ZW, Gao TT, Zhao Q, Ma FW, Li C. 2018. Long-term exogenous application of melatonin improves nutrient uptake fluxes in apple plants under moderate drought stress. Environ Exp Bot. 155:650–661. doi: 10.1016/j.envexpbot.2018.08.016
   Web of Science ®Google Scholar
• Liu J, Li Y, Wang W, Gai J, Li Y. 2016. Genome-wide analysis of MATE transporters and expression patterns of a subgroup of MATE genes in response to aluminum toxicity in soybean. BMC Genomics. 17:223. doi: 10.1186/s12864-016-2559-8
   PubMed Web of Science ®Google Scholar
• Maron LG, Pineros MA, Guimaraes CT, Magalhaes JV, Pleiman JK, Mao C, Shaff J, Belicuas SN, Kochian LV. 2010. Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. Plant J. 61:728–740. doi: 10.1111/j.1365-313X.2009.04103.x
   PubMed Web of Science ®Google Scholar
• Meng D, Gu Z, Li W, Wang A, Yuan H, Yang Q, Li T. 2014. Apple MdABCF assists in the transportation of S-RNase into pollen tubes. Plant J. 78:990–1002. doi: 10.1111/tpj.12524
   PubMed Web of Science ®Google Scholar
• Morita M, Shitan N, Sawada K, Van Montagu MC, Inze D, Rischer H, Goossens A, Oksman-Caldentey KM, Moriyama Y, Yazaki K. 2009. Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum. Proc Natl Acad Sci U S A. 106:2447–2452. doi: 10.1073/pnas.0812512106
   PubMed Web of Science ®Google Scholar
• Nawrath C, Heck S, Parinthawong N, Metraux JP. 2002. EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell. 14:275–286. doi: 10.1105/tpc.010376
   PubMed Web of Science ®Google Scholar
• Nesi N, Jond C, Debeaujon I, Caboche M, Lepiniec L. 2001. The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell. 13:2099–2114. doi: 10.1105/TPC.010098
   PubMed Web of Science ®Google Scholar
• Piddock LJ. 2006. Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin Microbiol Rev. 19:382–402. doi: 10.1128/CMR.19.2.382-402.2006
   PubMed Web of Science ®Google Scholar
• Pineau C, Loubet S, Lefoulon C, Chalies C, Fizames C, Lacombe B, Ferrand M, Loudet O, Berthomieu P, Richard O. 2012. Natural variation at the FRD3 MATE transporter locus reveals cross-talk between Fe homeostasis and Zn tolerance in Arabidopsis thaliana. PLoS Genet. 8:e1003120. doi: 10.1371/journal.pgen.1003120
   PubMed Web of Science ®Google Scholar
• Rogers EE, Guerinot ML. 2002. FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell. 14:1787–1799. doi: 10.1105/tpc.001495
   PubMed Web of Science ®Google Scholar
• Salunkhe DK, Chavan JK, Kadam SS. 1986. Pigeonpea as an important food source. Crit Rev Food Sci Nutr. 23:103–145. doi: 10.1080/10408398609527422
   PubMed Web of Science ®Google Scholar
• Santos ALD, Chaves-Silva S, Yang L, Maia LGS, Chalfun-Junior A, Sinharoy S, Zhao J, Benedito VA. 2017. Global analysis of the MATE gene family of metabolite transporters in tomato. BMC Plant Biol. 17:185. doi: 10.1186/s12870-017-1115-2
   PubMed Web of Science ®Google Scholar
• Seo PJ, Park J, Park MJ, Kim YS, Kim SG, Jung JH, Park CM. 2012. A Golgi-localized MATE transporter mediates iron homoeostasis under osmotic stress in Arabidopsis. Biochem J. 442:551–561. doi: 10.1042/BJ20111311
   PubMed Web of Science ®Google Scholar
• Shitan N, Kato K, Shoji T. 2014. Alkaloid transporters in plants. Plant Biotechnol. 31:453–463. doi: 10.5511/plantbiotechnology.14.1002a
   Web of Science ®Google Scholar
• Shitan N, Minami S, Morita M, Hayashida M, Ito S, Takanashi K, Omote H, Moriyama Y, Sugiyama A, Goossens A, et al. 2014. Involvement of the leaf-specific multidrug and toxic compound extrusion (MATE) transporter Nt-JAT2 in vacuolar sequestration of nicotine in Nicotiana tabacum. PLoS ONE. 9:e108789. doi: 10.1371/journal.pone.0108789
   PubMed Web of Science ®Google Scholar
• Shoji T, Inai K, Yazaki Y, Sato Y, Takase H, Shitan N, Yazaki K, Goto Y, Toyooka K, Matsuoka K, et al. 2008. Multidrug and toxic compound extrusion-type transporters implicated in vacuolar sequestration of nicotine in tobacco roots. Plant Physiol. 149:708–718. doi: 10.1104/pp.108.132811
   PubMed Web of Science ®Google Scholar
• Smith MA, Dauk M, Ramadan H, Yang H, Seamons LE, Haslam RP, Beaudoin F, Ramirez-Erosa I, Forseille L. 2013. Involvement of Arabidopsis Acyl-Coenzyme a desaturase-like2 (At2g31360) in the biosynthesis of the very-long-chain monounsaturated fatty acid components of membrane lipids. Plant Physiol. 161:81–96. doi: 10.1104/pp.112.202325
   PubMed Web of Science ®Google Scholar
• Thompson EP, Wilkins C, Demidchik V, Davies JM, Glover BJ. 2010. An Arabidopsis flavonoid transporter is required for anther dehiscence and pollen development. J Exp Bot. 61:439–451. doi: 10.1093/jxb/erp312
   PubMed Web of Science ®Google Scholar
• Varshney RK, Chen W, Li Y, Bharti AK, Saxena RK, Schlueter JA, Donoghue MT, Azam S, Fan G, Whaley AM, et al. 2012. Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat Biotechnol. 30:83–89. doi: 10.1038/nbt.2022
   Web of Science ®Google Scholar
• Vision TJ, Brown DG, Tanksley SD. 2000. The origins of genomic duplications in Arabidopsis. Science. 290:2114–2117. doi: 10.1126/science.290.5499.2114
   PubMed Web of Science ®Google Scholar
• Wang J, Hou Q, Li P, Yang L, Sun X, Benedito VA, Wen J, Chen B, Mysore KS, Zhao J. 2017. Diverse functions of multidrug and toxin extrusion (MATE) transporters in citric acid efflux and metal homeostasis in Medicago truncatula. Plant J. 90:79–95. doi: 10.1111/tpj.13471
   PubMed Web of Science ®Google Scholar
• Wang Z, Qian C, Guo X, Liu E, Mao K, Mu C, Chen N, Zhang W, Liu H. 2016. ELS1, a novel MATE transporter related to leaf senescence and iron homeostasis in Arabidopsis thaliana. Biochem Biophys Res Commun. 476:319–325. doi: 10.1016/j.bbrc.2016.05.121
   PubMed Web of Science ®Google Scholar
• Wu X, Li R, Shi J, Wang J, Sun Q, Zhang H, Xing Y, Qi Y, Zhang N, Guo YD. 2014. Brassica oleracea MATE encodes a citrate transporter and enhances aluminum tolerance in Arabidopsis thaliana. Plant Cell Physiol. 55:1426–1436. doi: 10.1093/pcp/pcu067
   PubMed Web of Science ®Google Scholar
• Yokosho K, Yamaji N, Fujii-Kashino M, Ma JF. 2016. Functional analysis of a MATE gene OsFRDL2 revealed its involvement in Al-induced secretion of citrate, but a lower contribution to Al tolerance in rice. Plant Cell Physiol. 57:976–985. doi: 10.1093/pcp/pcw026
   PubMed Web of Science ®Google Scholar
• Yokosho K, Yamaji N, Ma JF. 2016. OsFRDL1 expressed in nodes is required for distribution of iron to grains in rice. J Exp Bot. 67:5485–5494. doi: 10.1093/jxb/erw314
   PubMed Web of Science ®Google Scholar
• Zhao J, Dixon RA. 2009. MATE transporters facilitate vacuolar uptake of epicatechin 3'-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell. 21:2323–2340. doi: 10.1105/tpc.109.067819
   PubMed Web of Science ®Google Scholar
• Zhou G, Delhaize E, Zhou M, Ryan PR. 2013. The barley MATE gene, HvAACT1, increases citrate efflux and Al(3+) tolerance when expressed in wheat and barley. Ann Bot. 112:603–612. doi: 10.1093/aob/mct135
   PubMed Web of Science ®Google Scholar