Abstract
With the increasing acidification of soil, aluminum (Al) toxicity has become one of the most important stress factors affecting seed germination quality and crop yield. To investigate the Al tolerance on seed germination, genome-wide association analysis (GWAS) of 19,949 SNPs with genome-wide coverage was used to identify the candidate genes, which were potentially related to germinate traits of rapeseed (Brassica napus L.) under Al stress. In the experiment, 169 rapeseed cultivars (lines) were treated with AlCl3 solution of 90 ppm, and distilled water was added to the control. At the 7th day, the phenotype data, including root length and dry weight, were measured and calculated. Using the TASSEL software, Al tolerance related traits were explored in rapeseed under germination with a 60 K Brassica Illumina® Infinium SNP array. Then, the structure of the population was analyzed with the STRUCTURE software, and the genetic relationship and LD attenuation were analyzed with the software TASSEL, respectively. The GWAS of relative root length (RRL) and relative dry weight (RDW) with SNP markers were carried out under the optimal model. Meanwhile, the candidate genes were predicted based on the LD interval sequence of the associated SNP locus. Subsequently, the homologous genes of rapeseed related to Al tolerance in the target genome region were screened in Arabidopsis thaliana (L.) Heynh. The results showed that 13 SNPs were significantly associated with these two traits. Among them, 8 SNPs were significantly associated with RRL and located on chromosomes A03, A07, A09, A10, C05, C06, and C09, respectively. Five SNPs were significantly associated with RDW and located on chromosomes A03, A04, A10, C05, and C07, respectively. Afterward, fifty-nine candidate genes related to Al tolerance were identified in the LD region of these SNP loci. Four of these genes were involved in the growth regulation about organic acid, ten were involved in growth-regulating substance, eleven were related to oxidative stress, and nineteen were involved in carbon and nitrogen metabolism. The results of this study provided a theoretical basis for Al tolerance in rapeseed and laid out a foundation for further functional verification of genes and cultivation of new Al tolerant rapeseed varieties.
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Agrawal GK, Jwa NS, Shibato J, Han O, Iwahashi H, Rakwal R (2003) Diverse environmental cues transiently regulate OsOPR1 of the “octadecanoid pathway” revealing its importance in rice defense/stress and development. Biochem Biophys Res Commun 310(4):1073–1082. https://doi.org/10.1016/j.bbrc.2003.09.123. PMID: 14559225
Angeles-Núñez JG, Tiessen A (2010) Arabidopsis sucrose synthase 2 and 3 modulate metabolic homeostasis and direct carbon towards starch synthesis in developing seeds. Planta 232(3):701–718. https://doi.org/10.1007/s00425-010-1207-9
Anne P, Amiguet-Vercher A, Brandt B, Kalmbach L, Geldner N, Hothorn M et al (2018) CLERK is a novel receptor kinase required for sensing of root-active CLE peptides in Arabidopsis. Development. https://doi.org/10.1242/dev.162354
Ascencio-Ibanez JT, Sozzani R, Lee TJ, Chu TM, Wolfinger RD, Cella R et al (2008) Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol 148(1):436–454. https://doi.org/10.1104/pp.108.121038
Atwell S, Huang YS, Vilhjálmsson Bjarni J, Willems G, Horton M, Li Y et al (2010) Genome-wide association study of 107 phenotypes in a common set of Arabidopsis thaliana inbred lines. Nature 465:627–631. https://doi.org/10.1038/nature08800. PMID: 20336072
Bai FW, Matton DP (2018) The Arabidopsis mitogen-activated protein kinase kinase kinase 20 (MKKK20) C-terminal domain interacts with MKK3 and harbors a typical DEF mammalian MAP kinase docking site. Plant Signal Behav 13(8):e1503498. https://doi.org/10.1080/15592324.2018.1503498
Bhamburdekar SB, Chavan PD (2011) Effect of some stresses on free proline content during pigeonpea (Cajanas cajan) seed germination. J Stress Physiol Biochem 7(3):235–241. https://doi.org/10.1007/s00425-011-1419-7
Blanco F, Garreton V, Frey N, Dominguez C, Perez-Acle T, Van der Straeten D et al (2005) Identification of npr1-dependent and independent genes early induced by salicylic acid treatment in Arabidopsis. Plant Mol Biol 59(6):927–944. https://doi.org/10.1007/s11103-005-2227-x
Bock KW, Honys D, Ward JM, Padmanaban S, Nawrocki EP, Hirschi KD et al (2006) Integrating membrane transport with male gametophyte development and function through transcriptomics. Plant Physiol 140:1151–1168. https://doi.org/10.1104/pp.105.074708
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Buckler ES (2007) TASSEL, software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. https://doi.org/10.1093/bioinformatics/btm308. PMID: 17586829
Buschmann H, Chan J, Sanchez-Pulido L, Andrade-Navarro MA, Doonan JH, Lloyd CW (2006) Microtubule-associated AIR9 recognizes the cortical division site at preprophase and cell-plate insertion. Curr Biol 16(19):1938–1943. https://doi.org/10.1016/j.cub.2006.08.028. PMID: 17027491
Cai SG, Wu DZ, Jabeen Z, Huang YQ, Huang YC, Zhang GP (2013) Genome-wide association analysis of aluminum tolerance in cultivated and tibetan wild barley. PLoS ONE 8:e69776. https://doi.org/10.1371/journal.pone.0069776PMCID:PMC3724880
Castilhos G, Júlia GF, Schneider ADB, Oliveira PHD, Nicoloso FT, Schetinger MRC et al (2011) Aluminum-stress response in oat genotypes with monogenic tolerance. Environ Exp Bot 74:114–121. https://doi.org/10.1016/j.envexpbot.2011.05.007
Cellier F, Conejero G, Ricaud L, Luu DT, Lepetit M, Gosti F et al (2004) Characterization of atCHX17, a member of the cation/H+ exchangers, CHX family, from Arabidopsis thaliana suggests a role in K+ homeostasis. Plant J 39(6):834–846. https://doi.org/10.1111/j.1365-313X.2004.02177.x
Cha JY, Barman DN, Kim MG, Kim WY (2015) Stress defense mechanisms of NADPH-dependent thioredoxin reductases (NTRs) in plants. Plant Signal Behav 10(5):e1017698. https://doi.org/10.1080/15592324.2015.1017698
Chan A, Carianopol C, Tsai AYL, Varatharajah K, Chiu RS, Gazzarrini S (2017) Corrigendum: SnRK1 phosphorylation of FUSCA3 positively regulates embryogenesis, seed yield, and plant growth at high temperature in Arabidopsis. J Exp Bot 68:5981–5981. https://doi.org/10.1093/jxb/erx379
Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43(1):265–285. https://doi.org/10.1146/annurev-genet-102108-134148. PMID: 19686081
Crouzet J, Trombik T, Fraysse AS, Boutry M (2006) Organization and function of the plant pleiotropic drug resistance ABC transporter family. FEBS Lett 580(4):1123–1130. https://doi.org/10.1016/j.febslet.2005.12.043
Danquah A, de Zelicourt A, Boudsocq M, Neubauer J, Frei Dit Frey N, Leonhardt N et al (2015) Identifification and characterization of an ABA-activated map kinase cascade in Arabidopsis thaliana. Plant J Cell Mol Biol 82(2):232–244. https://doi.org/10.1111/tpj.12808. PMID: 25720833
De Abreu-Neto JB, Turchetto-Zolet AC, De Oliveira LFV, Bodanese Zanettini MH, Margis-Pinheiro M (2013) Heavy metal associated isoprenylated plant protein (HIPP): characterization of a family of proteins exclusive of plants. FEBS J 280(7):1604–1616. https://doi.org/10.1111/febs.12159
Degenhardt J, Larsen PB, Howell SH, Kochian LV (1998) Aluminum resistance in the Arabidopsis mutantalr-104 is caused by an aluminum-induced increase in rhizosphere pH. Plant Physiol 117:19–27. https://doi.org/10.1104/pp.117.1.19. PMID: 9576770
Ditt RF, Kerr KF, Figueiredo PD, Delrow J, Comai L, Nester EW (2006) The Arabidopsis thaliana transcriptome in response to agrobacterium tumefaciens. Mol Plant Microbe Interact 19(6):665–681. https://doi.org/10.1094/MPMI-19-0665
Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein s-glutathionylation in Arabidopsis. Plant Physiol 138(4):2233–2244. https://doi.org/10.1104/pp.104.058917
Doncheva S, Amenós M, Poschenrieder C, Barceló J (2005) Root cell patterning, a primary target for aluminum toxicity in maize. J Exp Bot 56:1213–1220. https://doi.org/10.1093/jxb/eri115. PMID: 15737983
Dong W, Wang M (2013) Wheat oxophytodienoate reductase gene TaOPR1 confers salinity tolerance via enhancement of abscisic acid signaling and reactive oxygen species scavenging. Plant Physiol 161:1217–1228
Doskocilova A, Plihal O, Volc J, Chumova J, Kourova H, Halada P et al (2011) A nodulin/glutamine synthetase-like fusion protein is implicated in the regulation of root morphogenesis and in signalling triggered by flagellin. Planta 234(3):459–476. https://doi.org/10.1007/s00425-011-1419-7. PMID: 21533644
Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER, a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Enders TA, Frick EM, Strader LC (2017) An Arabidopsis kinase cascade inflfluences auxin-responsive cell expansion. Plant J 92:68–81. https://doi.org/10.1111/tpj.13635. PMID: 28710770
Estornell LH, Landberg K, Cierlik I, Sundberg E (2018) SHI/STY genes affect Pre- and Post-meiotic anther processes in auxin sensing domains in Arabidopsis. Front Plant Sci 9:150. https://doi.org/10.3389/fpls.2018.00150
Exley C (2009) Darwin, natural selection and the biological essentiality of aluminum and silicon. Trends Biochem Sci 34:589–593. https://doi.org/10.1016/j.tibs.2009.07.006. PMID: 19773172
Fourcroy P, Tissot N, Gaymard F, Briat JF, Dubos C (2016) Facilitated Fe nutrition by phenolic compounds excreted by the Arabidopsis ABCG37/PDR9 transporter requires the IRT1/FRO2 high-affinity root Fe2+ transport. Mol Plant 9:485–488. https://doi.org/10.1016/j.molp.2015.09.010. PMID: 26415695
Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K et al (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091. https://doi.org/10.1093/pcp/pcm091
Gangl R, Tenhaken R (2016) Raffinose family oligosaccharides act as galactose storesin seeds and are required for rapid germination of Arabidopsisin the dark. Front Plant Sci 7:1115. https://doi.org/10.3389/fpls.2016.01115
Gao HH, Ye S, Wang Q, Wang LY, Wang RL, Chen LY, Tang ZL, Li JN, Zhou QY, Cui C (2019) Screening and comprehensive evaluation of aluminum-toxicity tolerance during seed germination in Brassca napus. Acta Agron Sin 45:1416–1430 (in Chinese with English abstract)
Giacomelli L, Rota-Stabelli O, Masuero D, Acheampong AK, Moretto M, Caputi L, Vrhovsek U, Moser C (2013) Gibberellin metabolism in Vitis vinifera L. during bloom and fruit-set:functional characterization and evolution of grapevine gibberellin oxidases. J Exp Bot 64(14):4403–4419. https://doi.org/10.1093/jxb/ert251
Gourley LM, Rogers SA, Ruiz-Gomez C, Clark RB (1990) Genetic aspects of aluminum tolerance in sorghum. Plant Soil 123:211–216. https://doi.org/10.1007/BF00011270
Gupta PK, Kulwal PL, Jaiswal V (2014) Association mapping in crop plants: opportunities and challenges. Adv Genet 85:109–148. https://doi.org/10.1016/B978-0-12-800271-1.00002-0. PMID: 24880734
Hamel F, Breton C, Houde M (1998) Isolation and characterization of wheat aluminum-regulated genes: possible involvement of aluminum as a pathogenesis response elicitor. Planta 205:531–538. https://doi.org/10.1007/s004250050352. PMID: 9684357
Hanada K, Sawada Y, Kuromori T, Klausnitzer R, Saito K, Toyoda T et al (2011) Functional compensation of primary and secondary metabolites by duplicate genes in Arabidopsis thaliana. Mol Biol Evol 28(1):377–382. https://doi.org/10.1093/molbev/msq204
Hatzig SV, Frisch M, Breuer F, Nesi N, Ducournau S, Wagner MH et al (2015) Genome-wide association mapping unravels the genetic control of seed germination and vigor in Brassica napus. Front Plant Sci 6:221. https://doi.org/10.3389/fpls.2015.00221. PMID: 25914704
He YJ, Wu DM, Wei DY, Fu Y, Cui YX, Dong HL et al (2017) Gwas, qtl mapping, and gene expression analyses in Brassica napus reveal genetic control of branching morphogenesis. Sci Rep UK 7:15971. https://doi.org/10.1038/s41598-017-15976-4. PMID: 29162897
Huang J, Zhang JH, Li WZ, Hu W, Duan LC, Feng Y et al (2013a) Genome-wide association analysis of ten chilling tolerance indices at the germination and seedling stages in maize. J Integr Plant Biol 55:735–744. https://doi.org/10.1111/jipb.12051. PMID: 23551400
Huang SM, Deng LB, Guan M, Li JN, Lu K, Wang HZ et al (2013b) Identification of genome-wide single nucleotide polymorphisms in allopolyploid crop Brassica napus. BMC Genom 14:717. https://doi.org/10.1186/1471-2164-14-717. PMID: 24138473
Inostroza-Blancheteau C, Aquea F, Reyes-Díaz M, Alberdi M, Arce-Johnson P (2011) Identification of aluminum-regulated genes by cDNA-AFLP analysis of roots in two contrasting genotypes of highbush blueberry (Vaccinium corymbosum L.). Mol Biotechnol 49(1):32–41. https://doi.org/10.1007/s12033-010-9373-3. PMID: 21225377
Jain M, Nagar P, Sharma A, Batth R, Aggarwal S, Kumari S et al (2018) GLYI and D-LDH play key role in methylglyoxal detoxification and abiotic stress tolerance. Sci Rep 8:5451. https://doi.org/10.1038/s41598-018-23806-4
Jiang L, Chen ZP, Gao QC, Ci LK, Cao SQ, Han Y et al (2016) Loss-of-function mutations in the APX1 gene result in enhanced selenium tolerance in Arabidopsis thaliana. Plant Cell Environ 39(10):2133–2144. https://doi.org/10.1111/pce.12762
Jost R, Altschmied L, Bloem E, Bogs J, Gershenzon J, Hahnel U et al (2005) Expression profiling of metabolic genes in response to methyl jasmonate reveals regulation of genes of primary and secondary sulfur-related pathways in Arabidopsis thaliana. Photosynth Res 86(3):491–508. https://doi.org/10.1007/s11120-005-7386-8
Kaya H, Takeda S, Kobayashi MJ, Kimura S, Iizuka A, Imai A et al (2019) Comparative analyses of the reactive oxygen species-producing enzymatic activity of Arabidopsis NADPH oxidases. Plant J 98(2):291–300. https://doi.org/10.1111/tpj.14212
Khare D, Mitsuda N, Lee S, Song WY, Hwang D, Ohme-Takagi M et al (2017) Root avoidance of toxic metals requires the GeBP-LIKE 4 transcription factor in Arabidopsis thaliana. New Phytol 213(3):1257–1273. https://doi.org/10.1111/nph.14242
Kihara T, Ohno T, Koyama H, Sawafuji T, Hara T (2003) Characterization of NADP-isocitrate dehydrogenase expression in a carrot mutant cell line with enhanced citrate excretion. Plant Soil 248:145–153. https://doi.org/10.1023/a:1022383426356
Kim J, Shiu SH, Thoma S, Li WH, Patterson SE (2006) Patterns of expansion and expression divergence in the plant polygalacturonase gene family. Genome Biol 7(9):87. https://doi.org/10.1186/gb-2006-7-9r87
Kim J, Sharkhuu A, Jin JB, Li PH, Jeong JC, Baek D et al (2007) yucca6, a dominant mutation in Arabidopsis, affects auxin accumulation and auxin-related phenotypes. Plant Physiol 145(3):722–735. https://doi.org/10.1104/pp.107.104935
Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260. https://doi.org/10.1146/annurev.pp.46.060195.001321
Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Physiol Plant Mol Biol 55:459–493. https://doi.org/10.1146/annurev.arplant.55.031903.141655
Kochian LV, Piñeros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195. https://doi.org/10.1007/1-4020-4099-7_9
Kochian LV, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:57–598. https://doi.org/10.1146/annurev-arplant-043014-114822. PMID: 25621514
Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL et al (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22(2623–2633):701. PMID: 12773379
Lee DH, Lal NK, Lin ZJD, Ma SS, Liu J, Castro B et al (2020) Regulation of reactive oxygen species during plant immunity through phosphorylation and ubiquitination of RBOHD. Nat Commun 11(1):1838. https://doi.org/10.1038/s41467-020-15601-5. PMID: 32296066
Li M, Qin R, Jiang W, Liu D (2015) Cytogenetical effects of aluminum on root meristem cells of Helianthus annuus L. Bot Sci 93:1–8. https://doi.org/10.17129/botsci.230
Li F, Chen BY, Xu K, Gao GZ, Yan GX, Qiao JW et al (2016) A genome-wide association study of plant height and primary branch number in rapeseed (Brassica napus). Plant Sci 242:169–177. https://doi.org/10.1016/j.plantsci.2015.05.012. PMID: 26566834
Li Y, Cai H, Liu P, Wang C, Gao H, Wu C et al (2017) Arabidopsis MAPKKK18 positively regulates drought stress resistance via downstream MAPKK3. Biochem Biophys Res Commun 484:292–297. https://doi.org/10.1016/j.bbrc.2017.01.104. PMID: 28131829
Li DH, Dossa K, Zhang YX, Wei X, Wang LH, Zhang YJ et al (2018) GWAS uncovers differential genetic bases for drought and salt tolerances in sesame at the germination stage. Genes 9:87. https://doi.org/10.3390/genes9020087. PMID: 29443881
Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD et al (2010) Acyl-lipid metabolism. Arabidopsis Book 8:e0133. https://doi.org/10.1199/tab.0133
Liu S, Wang J, Wang L, Wang X, Xue Y, Wu P et al (2009) Adventitious root formation in rice requires OsGNOM1 and is mediated by the OsPINs family. Cell Res 19:1110–1119. https://doi.org/10.1038/cr.2009.70. PMID: 19546891
Liu S, Fan CC, Li JN, Cai GQ, Yang QY, Wu J et al (2016) A genome-wide association study reveals novel elite allelic variations in seed oil content of Brassica napus. Theor Appl Genet 129:1203–1215. https://doi.org/10.1007/s00122-016-2697-z. PMID: 26912143
Lou HQ, Fan W, Jin JF, Xu JM, Chen WW, Yang JL et al (2020) A NAC-type transcription factor confers aluminum resistance by regulating cell wall-associated receptor kinase 1 and cell wall pectin. Plant Cell Environ 43:463–478. https://doi.org/10.1111/pce.13676. PMID: 31713247
Lu K, Wang TY, Xu XF, Tang ZL, Qu CM, He B et al (2016) Genome-wide association analysis of the height of podding and thickness of pod canopy in Brassica napus. Acta Agron Sin 42:344–352 (in Chinese with English abstract)
Luo Q, Zhao Z, Li DK, Zhang Y, Yang Y (2016) Overexpression of NaKR3 enhances salt tolerance in Arabidopsis. Genet Mol Res 15(1):15016378. https://doi.org/10.4238/gmr.15016378
Magadlela A, Morcillo RJL, Kleinert A, Venter M, Steenkamp E, Valentine A (2019) Glutamate dehydrogenase is essential in the acclimation of Virgilia divaricata, a legume indigenous to the nutrient-poor Mediterranean-type ecosystems of the Cape Fynbos. J Plant Physiol 43:153053. https://doi.org/10.1016/j.jplph.2019.153053
Magalhaes JV, Liu J, Guimarães CT, Lana UGP, Alves VMC, Wang YH et al (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in Sorghum. Nat Genet 39:1156–1161. https://doi.org/10.1038/ng2074. PMID: 17721535
Malinova I, Mahlow S, Alseekh S, Orawetz T, Fernie AR, Baumann O et al (2014) Double knockout mutants of Arabidopsis grown under normal conditions reveal that the plastidial phosphorylase isozyme participates in transitory starch metabolism. Plant Physiol 164(2):907–921. https://doi.org/10.1104/pp.113.227843
Marchi L, Polverini E, Degola F, Baruffini E, Restivo FM (2014) Glutamate dehydrogenase isoenzyme 3 (GDH3) of Arabidopsis thaliana is less thermostable than GDH1 and GDH2 isoenzymes. Plant Physiol Biochem 83:225–231. https://doi.org/10.1016/j.plaphy.2014.08.003. PMID: 25180813
Marciano DPRO, Ramos FT, Alvim MN, Magalhaes JR, Franca MGC (2010) Nitric oxide reduces the stress effects of aluminum on the process of germination and early root growth of rice. J Plant Nutr Soil Sci 173:885–891. https://doi.org/10.1002/jpln.200900312
Maser P, Thomine S, Schroeder J, Ward JM, Hirschi K, Sze H et al (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126(4):1646–1667. https://doi.org/10.1104/pp.126.4.1646
Mattiello L, Da SF, Menossi M (2012) Linking microarray data to QTLs highlights new genes related to al tolerance in maize. Plant Sci 191–192:8–15. https://doi.org/10.1016/j.plantsci.2012.04.009. PMID: 22682560
McCoy JG, Arabshahi A, Bitto E, Bingman CA, Ruzicka FJ, Frey PA et al (2006) Structure and mechanism of an ADP-glucose phosphorylase from Arabidopsis thaliana. Biochemistry 45(10):3154–3162. https://doi.org/10.1021/bi052232m. PMID: 16519510
Melotto M (2008) A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine-and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein. Plant J 55:979–988. https://doi.org/10.1111/j.1365-313X.2008.03566.x. PMID: 18547396
Meng LJ, Wang BX, Zhao XQ, Ponce K, Qian Q, Ye GY (2017) Association mapping of ferrous, zinc and aluminum tolerance at the seedling stage in Indica rice using MAGIC populations. Front Plant Sci 8:1822. https://doi.org/10.3389/fpls.2017.01822PMID:29123537. PMID: 29123537
Meng L, Zhang T, Geng S, Scott PB, Li H, Chen S (2019) Comparative proteomics and metabolomics of JAZ7-mediated drought tolerance in Arabidopsis. J Proteom 196:81–91. https://doi.org/10.1016/j.jprot.2019.02.001
Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V et al (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal. https://doi.org/10.1126/scisignal.2000448. PMID: 19690331
Min X, Jin X, Liu W, Wei X, Zhang Z, Ndayambaza B, Wang Y (2019) Transcriptome-wide characterization and functional analysis of MATE transporters in response to aluminum toxicity in Medicago sativa L. Peer J 7:e6302. https://doi.org/10.7717/peerj.6302. PMID: 30723620
Murgia I, Tarantino D, Soave C, Morandini P (2011) Arabidopsis CYP82C4 expression is dependent on Fe availability and circadian rhythm and correlates with genes involved in the early Fe deficiency response. J Plant Physiol 168:894–902. https://doi.org/10.1016/j.jplph.2010.11.020. PMID: 21315474
Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475. https://doi.org/10.1016/j.cell.2006.05.050
Nguyen VT, Burow MD, Nguyen HT, Le BT, Le TD, Paterson AH (2001) Molecular mapping of genes conferring aluminum tolerance in rice (oryza sativa L.). Theor Appl Genet 102:1002–1010. https://doi.org/10.1007/s001220000472
Ohyama K, Ogawa M, Matsubayashi Y (2008) Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant J 55(1):152–160. https://doi.org/10.1111/j.1365-313X.2008.03464.x
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. PMID:10835412
Qian P, Sun R, Basharat B, Bullet A, Zhou W (2014) Effects of hydrogen sulfide on growth, antioxidative capacity, and ultrastructural changes in oilseed rape seedlings under aluminum toxicity. J Plant Growth Regul 33:526–538. https://doi.org/10.1007/s00344-013-9402-0
Ren YB, Cao JS, Miao M, Meng Y, Fan TT, Cao SQ et al (2018) DFR1-mediated inhibition of proline degradation pathway regulates drought and freezing tolerance in Arabidopsis. Cell Rep 23(13):3960–3974. https://doi.org/10.1016/j.celrep.2018.04.011
Rieu I, Eriksson S, Powers SJ, Gong F, Griffiths J, Woolley L et al (2008a) Genetic analysis reveals that C-19-GA 2-Oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell 20:2420–2436. https://doi.org/10.1105/tpc.108.058818
Rieu I, Ruiz-Rivero O, Fernandez-Garcia N, Powers J, Gong SJ, Linhartova F et al (2008b) The gibberellin biosynthetic genes ATGA20ox1 and ATGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle. Plant J 53(3):488–504. https://doi.org/10.1111/j.1365-313X.2007.03356.x
Rockwell NC, Wolfger H, Kuchler K, Thorner J (2009) ABC transporter Pdr10 regulates the membrane microenvironment of Pdr12 in saccharomyces cerevisiae. J Membr Biol 229(1):27–52. https://doi.org/10.1007/s00232-009-9173-5. PMID: 19452121
Ryan PR (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Biol 52:527–560. https://doi.org/10.1146/annurev.arplant.52.1.527. PMID: 11337408
Ryan PR, Delhaize E (2010) The convergent evolution of aluminum resistance in plants exploits a convenient currency. Funct Plant Biol 37:275–284. https://doi.org/10.1071/FP09261
Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E (2009) A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol 149:340–351. https://doi.org/10.1104/pp.108.129155. PMID: 19005085
Sade H, Meriga B, Surapu V, Gadi J, Sunita MS, Suravajhala P, Kavi Kishor PB (2016) Toxicity and tolerance of aluminum in plants: tailoring plants to suit to acid soils. Biol Met 29(2):187–210. https://doi.org/10.1007/s10534-016-9910-z. PMID: 26796895
Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Millar AH et al (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes result in altered metabolic sensitivity to oxidative stress. Plant J 58:53–68. https://doi.org/10.1111/j.1365-313x.2008.03761.x
Sardar A, Nandi AK, Chattopadhyay D (2017) CBL-interacting protein kinase 6 negatively regulates immune response to pseudomonas syringae in Arabidopsis. J Exp Bot 68(13):3573–3584. https://doi.org/10.1093/jxb/erx170. PMID: 28541442
Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V et al (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6(7):2180–2198. https://doi.org/10.1002/pmic.200500543
Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR et al (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653. https://doi.org/10.1111/j.1365-313x.2003.01991.x. PMID: 14871306
Shi YY, Gao LL, Wu ZC, Zhang XJ, Wang MM, Zhang CS et al (2017) Genome-wide association study of salt tolerance at the seed germination stage in rice. BMC Plant Biol 17:92. https://doi.org/10.1186/s12870-017-1044-0. PMID: 28558653
Shu K, Liu XD, Xie Q, He ZH (2016) Two faces of one seed: hormonal regulation of dormancy and germination. Mol Plant 9:34. https://doi.org/10.1016/j.molp.2015.08.010. PMID: 26343970
Silva P, Matos M (2016) Assessment of the impact of Aluminum on germination, early growth and free proline content in Lactuca sativa L. Ecotoxicol Environ Saf 131:151–156. https://doi.org/10.1016/j.ecoenv.2016.05.014. PMID: 27229755
Smart SVDBC (2002) The plant PDR family of ABC transporters. Planta 216:95–106. https://doi.org/10.1007/s00425-002-0889-z. PMID: 12430018
Spartz AK, Lee SH, Wenger JP, Gonzalez N, Itoh H, Inzé D et al (2012) The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant J 70(6):978–990. https://doi.org/10.1111/j.1365-313X.2012.04946.x. PMID: 22348445
Strader LC, Bartel B (2009) The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell 21:1992–2007. https://doi.org/10.1105/tpc.109.065821. PMID: 19648296
Suzuki M, Sato Y, Wu S, Kang BH, Mccarty DR (2015) Conserved functions of the mate transporter big embryo1 in regulation of lateral organ size and initiation rate. Plant Cell 27(8):2288–2300. https://doi.org/10.1105/tpc.15.00290
Taguchi G, Ubukata T, Nozue H, Kobayashi Y, Takahi M, Yamamoto H et al (2010) Malonylation is a key reaction in the metabolism of xenobiotic phenolic glucosides in Arabidopsis and tobacco. Plant J 63(6):1031–1041. https://doi.org/10.1111/j.1365-313X.2010.04298.x
Tan M, Liao F, Hou L, Wang J, Wei L, Jian H et al (2017) Genome-wide association analysis of seed germination percentage and germination index in Brassica napus L. under salt and drought stresses. Euphytica 213:40. https://doi.org/10.1007/s10681-016-1832-x
Tang QY, Zhang CX (2013) Data Processing System (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Sci 20:254–260. https://doi.org/10.1111/j.1744-7917.2012.01519.x. PMID: 23955865
Tao YH, Niu YN, Wang Y, Chen TX, Amir NS, Zhang J et al (2018) Genome-wide association mapping of aluminum toxicity tolerance and fine mapping of a candidate gene for nrat1 in rice. PLoS ONE 13:e0198589. https://doi.org/10.1371/journal.pone.0198589. PMID: 29894520
Tehseen M, Cairns N, Sherson S, Cobbett CS (2010) Metallochaperone-like genes in Arabidopsis thaliana. Metallomics Integr Biomet Sci 2(8):556–564. https://doi.org/10.1039/c003484c
Unterseer S, Bauer E, Haberer G, Seidel M, Knaak C, Ouzunova M et al (2014) A powerful tool for genome analysis in maize: development and evaluation of the high density 600 k snp genotyping array. BMC Genom 15:823. https://doi.org/10.1186/1471-2164-15-823. PMID: 25266061
Velasquez SM, Ricardi MM, Poulsen CP, Oikawa A, Dilokpimol A, Halim A (2015) Complex regulation of prolyl-4-hydroxylases impacts root hair expansion. Mol Plant 8(5):734–746. https://doi.org/10.1016/j.molp.2014.11.017. PMID: 25655826
Wang X, Zhang Y, Ma QB, Zhang ZL, Xue Y, Bao SL et al (2007) SKB1-mediated symmetric dimethylation of histone H4R3 controls flowering time in Arabidopsis. EMBO J 26(7):1934–1941. https://doi.org/10.1038/sj.emboj.7601647. PMID: 17363895
Wang R, Liu X, Liang S, Ge Q, Li Y, Shao J et al (2015) A subgroup of MATE transporter genes regulates hypocotyl cell elongation in Arabidopsis. J Exp Bot 66:6327. https://doi.org/10.1093/jxb/erv344. PMID: 26160579
Wang K, Guo Q, Froehlich JE, Hersh HL, Zienkiewicz A, Howe GA et al (2018) Two abscisic acid responsive plastid lipase genes involved in jasmonic acid biosynthesis in Arabidopsis thaliana. Plant Cell 30(5):1006–1022. https://doi.org/10.1105/tpc.18.00250
Wei LJ, Jian HJ, Lu K, Filardo F, Yin NW, Liu LZ et al (2016) Genome-wide association analysis and differential expression analysis of resistance to Sclerotinia stem rot in Brassica napus. Plant Biotechnol J 14:1368–1380. https://doi.org/10.1111/pbi.12501. PMID: 26563848
Wild M, Daviere JM, Cheminant S, Regnault T, Baumberger N, Heintz D et al (2012) The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell 24(8):3307–3319. https://doi.org/10.1105/tpc.112.101428
Wuddineh WA, Mazarei M, Zhang JY, Poovaiah CR, Mann DGJ, Ziebell A et al (2015) Identification and overexpression of gibberellin 2-oxidase (GA2ox) in switchgrass (Panicum virgatum L.) for improved plant architecture and reduced biomass recalcitrance. Plant Biotechnol J 13(5):636–647. https://doi.org/10.1111/pbi.12287. PMID: 25400275
Xu LP, Hu KN, Zhang ZQ, Guan CY, Chen S, Hua W et al (2016) Genome-wide association study reveal the genetic architecture of flowering time in rapeseed (Brassica napus L.). DNA Res 23:43. https://doi.org/10.1093/dnares/dsv035. PMID: 26659471
Xu JM, Wang ZQ, Jin JF, Chen WW, Fan W, Zheng SJ, Yang JL (2019) FeSTAR2 interacted by FeSTAR1 alters its subcellular location and regulates Al tolerance in buckwheat. Plant Soil 436:489–501
Xue YF, Chen BJ, Wang R, Win AN, Li JN, Chai YR (2018) Genome-wide survey and characterization of fatty acid desaturase gene family in Brassica napus and its parental species. Appl Biochem Biotechnol 184:582. https://doi.org/10.1007/s12010-017-2563-8. PMID: 28799009
Yan CX, Yan ZY, Wang YZ, Yan XY, Han YZ (2014) Tudor-SN, a component of stress granules, regulates growth under salt stress by modulating GA20ox3 mRNA levels in Arabidopsis. J Exp Bot 65(20):5933–5944. https://doi.org/10.1093/jxb/eru334
Yang SH, Yang HJ, Grisafi P, Sanchatjate S, Fink GR, Sun Q et al (2010) The BON/CPN gene family represses cell death and promotes cell growth in Arabidopsis. Plant J 45(2):166–179. https://doi.org/10.1111/j.1365-313X.2005.02585.x. PMID: 16367962
Yang JL, Fan W, Zheng SJ (2019) Mechanisms and regulation of aluminum-induced secretion of organic acid anions from plant roots. J Zhejiang Univ ENCE B 20(6):513–527. https://doi.org/10.1631/jzus.B1900188. PMID: 31090277
Yilmaz HM, Yakar M, Mutluoglu O, Kavurmaci MM, Yurt K (2012) Monitoring of soil erosion in cappadocia region(selime-aksaray-turkey). Environ Earth Sci 66(1):75–81. https://doi.org/10.1007/s12665-011-1208-4
Yoo CM, Quan L, Blancaflor EB (2012) Divergence and redundancy in CSLD2 and CSLD3 function during Arabidopsis thaliana root hair and female gametophyte development. Front Plant Sci 3:111. https://doi.org/10.3389/fpls.2012.00111
Yuriko K, Takashi I, Kazuhiko K, Orito Y, Hiroyuki K (2007) Characterisation of lanthanum toxicity for root growth of, Arabidopsis thaliana, from the aspect of natural genetic variation. Funct Plant Biol 34:984–994. https://doi.org/10.1071/FP07133
Zhai LM, Sun CH, Feng Y, Li DY, Chai XF, Wang L et al (2018) AtROP6 is involved in reactive oxygen species signaling in response to iron-deficiency stress in Arabidopsis thaliana. FEBS Lett 592(20):3446–3459. https://doi.org/10.1002/1873-3468.13257. PMID: 30238451
Zheng H, Zhang F, Wang S, Su Y, Ji X, Jiang P et al (2018a) MLK1 and MLK2 coordinate RGA and CCA1 activity to regulate hypocotyl elongation in Arabidopsisthaliana. Plant Cell 30:67–82. https://doi.org/10.1105/tpc.17.00830. PMID: 29255112
Zheng X, Chen L, Li X (2018b) Arabidopsis and rice showed a distinct pattern in ZIPs genes expression profile in response to Cd stress. Bot Stud. https://doi.org/10.1186/s40529-018-0238-6
Zhou SX, Chen MT, Zhang YB, Gao Q, Noman A, Wang Q et al (2019) OsMKK3, a stress-responsive protein kinase, positively regulates rice resistance to nilaparvata lugens via phytohormone dynamics. Int J Mol Sci 20(12):3023. https://doi.org/10.3390/ijms20123023 . PMID: 3
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This work was supported by the National Key Research and Development Program (2018YFD0100500), and the Chongqing Municipal Science and Technology Innovation Project (cstc2019jscx-msxm1538).
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Data curation: HG, SY. Formal analysis: HG. Funding acquisition: CC, QZ. Investigation: HG, SY, LW, RW, WL, JW, LM, FY. Project administration: CC, QZ. Supervision: CC, QZ. Writing—original draft: HG. Writing—review and editing: CC, QZ, JW.
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Gao, H., Ye, S., Wu, J. et al. Genome-wide association analysis of aluminum tolerance related traits in rapeseed (Brassica napus L.) during germination. Genet Resour Crop Evol 68, 335–357 (2021). https://doi.org/10.1007/s10722-020-00989-2
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DOI: https://doi.org/10.1007/s10722-020-00989-2