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QTL mapping for aluminum tolerance in RIL population of soybean (Glycine max L.) by RAD sequencing


Autoři: Xinxin Wang aff001;  Yanbo Cheng aff001;  Ce Yang aff001;  Cunyi Yang aff001;  Yinghui Mu aff001;  Qiuju Xia aff004;  Qibin Ma aff001
Působiště autorů: The State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, South China Agricultural University, Guangzhou, Guangdong, China aff001;  The Key Laboratory of Plant Molecular Breeding of Guangdong Province, College of Agriculture, South China Agricultural University, Guangzhou, Guangdong, China aff002;  The National Engineering Research Center of Plant Space Breeding, South China Agricultural University, Guangzhou, Guangdong, China aff003;  The Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, China aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223674

Souhrn

Aluminum (Al3+) toxicity is a typical abiotic stress that severely limits crop production in acidic soils. In this study, an RIL (recombinant inbred line, F12) population derived from the cross of Zhonghuang 24 (ZH 24) and Huaxia 3 (HX 3) (160 lines) was tested using hydroponic cultivation. Relative root elongation (RRE) and apical Al3+ content (AAC) were evaluated for each line, and a significant negative correlation was detected between the two indicators. Based on a high-density genetic linkage map, the phenotypic data were used to identify quantitative trait loci (QTLs) associated with these traits. With composite interval mapping (CIM) of the linkage map, five QTLs that explained 39.65% of RRE and AAC variation were detected on chromosomes (Chrs) Gm04, Gm16, Gm17 and Gm19. Two new QTLs, qRRE_04 and qAAC_04, were located on the same region of bin93-bin94 on Chr Gm04, which explained 7.09% and 8.98% phenotypic variation, respectively. Furthermore, the results of the expression analysis of candidate genes in the five genetic regions of the QTLs showed that six genes (Glyma.04g218700, Glyma.04g212800, Glyma.04g213300, Glyma.04g217400, Glyma.04g216100 and Glyma.04g220600) exhibited significant differential expression between the Al3+ treatment and the control of two parents. The results of qRT-PCR analysis indicated that Glyma.04g218700 was upregulated by Al3+ treatment with the hundreds-fold increased expression level and may be a candidate gene with potential roles in the response to aluminum stress. Therefore, our efforts will enable future functional analysis of candidate genes and will contribute to the strategies for improvement of aluminum tolerance in soybean.

Klíčová slova:

Aluminum – Gene expression – Gene mapping – Genetic linkage – Linkage mapping – Plant resistance to abiotic stress – Quantitative trait loci – Soybean


Zdroje

1. Guo JH, Liu XJ, Zhang Y, Shen JL, Man WX, Zhang WF, et al. Significant acidification in major Chinese croplands. Science. 2010;327(5968): 1008–1010. doi: 10.1126/science.1182570 20150447

2. Kochian LV, Hoekenga OA, Pineros MA. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Ann Rev Plant Biol. 2004;55(1): 459–493.

3. Delhaize E, Ryan PR. Aluminum toxicity and tolerance in plants. Plant Physiol. 1995;107(2): 315–321. doi: 10.1104/pp.107.2.315 12228360

4. Yamamoto Y. Aluminum toxicity in plant cells: Mechanisms of cell death and inhibition of cell elongation. Soil Sci Plant Nutr. 2018;65(1): 41–55.

5. Kochian LV, Piñeros MA, Hoekenga OA. The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil. 2005;274(1–2): 175–195.

6. Matsumoto H. Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol. 2000;200(200): 1.

7. Miyasaka SC, Hawes MC. Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol. 2001;125(4): 1978–1987. doi: 10.1104/pp.125.4.1978 11299377

8. Inostroza-Blancheteau C, Rengel Z, Alberdi M, de la Luz Mora M, Aquea F, Arce-Johnson P, et al. Molecular and physiological strategies to increase aluminum resistance in plants. Mol Bio Rep. 2012;39(3): 2069–2079.

9. Ma JF, Hiradate S, Nomoto K, Iwashita T, Matsumoto H. Internal detoxification mechanism of al in hydrangea (identification of Al3+ form in the leaves). Plant Physiol. 1997;113(4): 1033–1039. doi: 10.1104/pp.113.4.1033 12223659

10. Foy CD, Duke JA, Devine TE. Tolerance of soybean germplasm to an acid Tatum subsoil. J Plant Nutr. 1992;15(5): 527–547.

11. Jena KK, Mackill DJ. Molecular markers and their use in marker-assisted selection in rice. Crop Sci. 2008;48(4): 1266.

12. Cai S, Dezhi W, Zahra J, Yuqing H, Yechang H, Guoping Z, et al. Genome-wide association analysis of aluminum tolerance in cultivated and Tibetan wild barley. PLoS One. 2013;8(7): e69776. doi: 10.1371/journal.pone.0069776 23922796

13. Mackay TF. The genetic architecture of quantitative traits. Annu Rev Genet. 2004;14(3): 253–257.

14. Kobayashi Y, Koyama H. QTL analysis of Al3+ tolerance in recombinant inbred lines of Arabidopsis thaliana. Plant Cell Physiol. 2002;43(12): 1526–1533. doi: 10.1093/pcp/pcf174 12514250

15. Wu P, Hu BYK, Jin WZ, Ni JJ, He C, Liao CY. QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor Appl Genet. 2000;100(8): 1295–1303.

16. Tao YH, Niu YN, Wang Y, Chen TX, Amir NS, Zhang J, et al. Genome-wide association mapping of aluminum toxicity tolerance and fine mapping of a candidate gene for Nrat1 in rice. PLoS One. 2018;13(6): e0198589. doi: 10.1371/journal.pone.0198589 29894520

17. Zhou L-L, Bai G-H, Ma H-X, Carver BF. Quantitative trait loci for aluminum resistance in wheat. Mol Breeding. 2006;19(2): 153–161.

18. Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E. A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol. 2009;149(1): 340–351. doi: 10.1104/pp.108.129155 19005085

19. Wang J, Raman H, Zhou M, Ryan PR, Delhaize E, Hebb DM, et al. High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminum tolerance in barley (Hordeum vulgare L.). Theor Appl Genet. 2007;115(2): 265–76. doi: 10.1007/s00122-007-0562-9 17551710

20. Guimaraes CT, Simoes CC, Pastina MM, Maron LG, Magalhaes JV, Vasconcellos RC, et al. Genetic dissection of Al3+ tolerance QTLs in the maize genome by high density SNP scan. BMC Genomics. 2014;15(1): 153.

21. Qi B, Korir P, Zhao T, Yu D, Chen S, Gai J. Mapping quantitative trait loci associated with aluminum toxin tolerance in NJRIKY recombinant inbred line population of soybean (Glycine max L). J Integr Plant Biol. 2008;50(9): 1089–1095. doi: 10.1111/j.1744-7909.2008.00682.x 18844777

22. Narasimhamoorthy B, Bouton JH, Olsen KM, Sledge MK. Quantitative trait loci and candidate gene mapping of aluminum tolerance in diploid alfalfa. Theor Appl Genet. 2007;114(5): 901–913. doi: 10.1007/s00122-006-0488-7 17219204

23. Bianchihall CM, Carter TE Jr, Bailey MA, Mian MAR, Rufty TW, Ashley DA, et al. Aluminum tolerance associated with quantitative trait loci derived from soybean PI 416937 in hydroponics. Crop Sci. 2000;40(2): 538–545.

24. Korir PC, Qi B, Wang Y, Zhao T, Yu D, Chen S, et al. A study on relative importance of additive, epistasis and unmapped QTL for Aluminium tolerance at seedling stage in soybean. Plant Breeding. 2011;130(5): 551–562.

25. Gai J, Ying L, Huineng LV, Han X, Zhao T, Deyue YU, et al. Identification, inheritance and QTL mapping of root traits related to tolerance to rhizo-spheric stresses in soybean (Glycine max (L.) Merr.). Frontiers of Agriculture in China. 2007;1(2): 119–128.

26. Liu Y. Identification of tolerance to aluminum toxin and inheritance of related root traits in soybeans (Glycine max (L) Merr.). Soybean Science. 2004;23(3): 164.

27. Huang X, Feng Q, Qian Q, Zhao Q, Wang L, Wang A, et al. High-throughput genotyping by whole-genome resequencing. Genome Res. 2009;19(6): 1068. doi: 10.1101/gr.089516.108 19420380

28. Chen H, Xie W, He H, Yu H, Chen W, Li J, et al. A high-density SNP genotyping array for rice biology and molecular breeding. Mol Plant. 2014;7(3): 541–553. doi: 10.1093/mp/sst135 24121292

29. Davey JW, Blaxter ML. RADSeq: next-generation population genetics. Brief Funct Genomics. 2010;9(5–6): 416–423. doi: 10.1093/bfgp/elq031 21266344

30. Schuster SC. Next-generation sequencing transforms today's biology. Nat methods. 2008;5(1): 16. doi: 10.1038/nmeth1156 18165802

31. Zhou L, Wang SB, Jian J, Geng QC, Wen J, Song Q, et al. Identification of domestication-related loci associated with flowering time and seed size in soybean with the RAD-seq genotyping method. Sci Rep. 2015;5: 9350. doi: 10.1038/srep09350 25797785

32. Cai Z, Cheng Y, Ma Z, Liu X, Ma Q, Xia Q, et al. Fine-mapping of QTLs for individual and total isoflavone content in soybean (Glycine max L.) using a high-density genetic map. Theor Appl Genet. 2018;131(3): 555–568. doi: 10.1007/s00122-017-3018-x 29159422

33. Poland JA, Brown PJ, Sorrells ME, Jannink JL. Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One. 2012;7(2): e32253. doi: 10.1371/journal.pone.0032253 22389690

34. Abdel-Haleem H, Carter TE, Rufty TW, Boerma HR, Li Z. Quantitative trait loci controlling aluminum tolerance in soybean: candidate gene and single nucleotide polymorphism marker discovery. Mol Breeding. 2014;33(4): 851–862.

35. Liu N, Li M, Hu X, Ma Q, Mu Y, Tan Z, et al. Construction of high-density genetic map and QTL mapping of yield-related and two quality traits in soybean RILs population by RAD-sequencing. BMC genomics. 2017;18(1): 466. doi: 10.1186/s12864-017-3854-8 28629322

36. Wang L, Cheng Y, Ma Q, Mu Y, Huang Z, Xia Q, et al. QTL fine-mapping of soybean (Glycine max L.) leaf type associated traits in two RILs populations. BMC Genomics. 2019;20(1): 260. doi: 10.1186/s12864-019-5610-8 30940069

37. BianchiHall CM, Carter TE, Rufty TW, Arellano C, Boerma HR, Ashley DA. Heritability and resource allocation of aluminum tolerance derived from soybean PI 416937. Crop Sci. 1998;38(2): 513–522.

38. Osawa H, Matsumoto H. Possible involvement of protein phosphorylation in aluminum-responsive malate efflux from wheat root apex. Plant Physiol. 2001;126(1): 411–420. doi: 10.1104/pp.126.1.411 11351103

39. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, et al. Genome sequence of the palaeopolyploid soybean. Nature. 2010;463(7278): 178–183. doi: 10.1038/nature08670 20075913

40. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics. 2009;25(15): 1966–1967. doi: 10.1093/bioinformatics/btp336 19497933

41. Voorrips RE. MapChart: Software for the graphical presentation of linkage maps and QTLs. Journal of hered. 2002;93(1): 77–78.

42. Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, et al. Soybean WRKY‐type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J. 2008;6(5): 486–503. doi: 10.1111/j.1467-7652.2008.00336.x 18384508

43. Wang Y, Yu K, Poysa V, Shi C, Zhou Y. Selection of reference genes for normalization of qRT-PCR analysis of differentially expressed genes in soybean exposed to cadmium. Mol Bio Rep. 2012;39(2): 1585–1594.

44. Ziegel ER. SAS System for Linear Models (3rd ed.). Technometrics. 1992;34(4): 500.

45. Knapp SJ, Stroup WW, Ross WM. Exact confidence intervals for heritability on a progeny mean basis. Crop Science. 1985;25(1): 192–194.

46. Du Z, Zhou X, Ling Y, Zhang Z, Su Z. AgriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 2010;38: W64. doi: 10.1093/nar/gkq310 20435677

47. Dall'Agnol M, Bouton JH, Parrott WA. Screening methods to develop alfalfa germplasms tolerant of acid, aluminum toxic soils. Crop Sci. 1996;181(88500): 64–70.

48. Villagarcia MR, Carter TE, Rufty TW, Niewoehner AS, Jennette MW, Arrellano C. Genotypic rankings for aluminum tolerance of soybean roots grown in hydroponics and sand culture. Crop Sci. 2001;41(5): 1499–1507.

49. Famoso AN, Clark RT, Shaff JE, Craft E, Mccouch SR, Kochian LV. Development of a novel aluminum tolerance phenotyping platform used for comparisons of cereal aluminum tolerance and investigations into rice aluminum tolerance mechanisms. Plant Physiol. 2010;153(4): 1678–1691. doi: 10.1104/pp.110.156794 20538888

50. Campbell KAG, Carter TE Jr. Aluminum tolerance in soybean: I. Genotypic correlation and repeatability of solution culture and greenhouse screening methods. Crop Sci. 1990;30(5): 1049–1054.

51. Ma JF, Zheng SJ, Li XF, Takeda K, Matsumoto H. A rapid hydroponic screening for aluminium tolerance in barley. Plant Soil. 1997;191(1): 133–137.

52. Baier AC, Somers DJ, Gustafson JP. Aluminium tolerance in wheat: correlating hydroponic evaluations with field and soil performances. Plant Breeding. 2010;114(4): 291–196.

53. Cai M, Liu P, Xu G. Response of root border cells to Al3+ toxicity in soybean. Scientia Agricultura Sinica. 2007;40(2): 271–276.

54. Ma JF, Shen R, Zhao Z, Wissuwa M, Takeuchi Y, Ebitani T, et al. Response of rice to Al3+ stress and identification of quantitative trait Loci for Al3+ tolerance. Plant Cell Physiol. 2002;43(6): 652–659. doi: 10.1093/pcp/pcf081 12091719

55. Ma HX, Bai GH, Carver BF, Zhou LL. Molecular mapping of a quantitative trait locus for aluminum tolerance in wheat cultivar Atlas 66. Theor Appl Genet. 2005;112(1): 51–57. doi: 10.1007/s00122-005-0101-5 16189660

56. Ryan P, Raman H, Gupta S, Sasaki T, Yamamoto Y, Delhaize M. The multiple origins of aluminium resistance in hexaploid wheat include Aegilops tauschii and more recent cis mutations to TaALMT1. Plant Journal. 2010;64(3): 446–55. doi: 10.1111/j.1365-313X.2010.04338.x 20804458

57. Kopittke PM, Menzies NW, Wang P, Blamey FP. Kinetics and nature of aluminium rhizotoxic effects: a review. Journal Exp Bot. 2016;67(15): erw233.

58. Sapra VT, Mebrahtu T, Mugwira LM. Soybean germplasm and cultivar aluminum tolerance in nutrient solution and Bladen clay loam soil 1. Agronomy Journal. 1982;74(4): 687–690.

59. Echart CL, Barbosa-Neto JF, Garvin DF, Cavalli-Molina S. Aluminum tolerance in barley: Methods for screening and genetic analysis. Euphytica. 2002;126(3): 309–313.

60. Dai SF, Yan ZH, Liu DC, Zhang LQ, Wei YM, Zheng YL. Evaluation on chinese bread wheat landraces for low pH and aluminum tolerance using hydroponic screening. Agr Sci China. 2009;8(3): 285–292.

61. Ma Q, Yi R, Li L, Liang Z, Zeng T, Zhang Y, et al. GsMATE encoding a multidrug and toxic compound extrusion transporter enhances aluminum tolerance in Arabidopsis thaliana. BMC Plant Biol. 2018;18(1): 212. doi: 10.1186/s12870-018-1397-z 30268093

62. Raman H, Zhang K, Cakir M, Appels R, Ryan PR. Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome. 2005;48(5): 781–791. doi: 10.1139/g05-054 16391684

63. Delhaize E, Ryan PR, Randall PJ. Aluminum Tolerance in Wheat (Triticum aestivum L.) (II. Aluminum-stimulated excretion of malic acid from root apices). Plant Physiol. 1993;103(3): 695–702. doi: 10.1104/pp.103.3.695 12231973

64. Geng X, Horst WJ, Golz JF, Lee JE, Ding Z, Yang ZB. Leunig_homolog transcriptional co‐repressor mediates aluminium sensitivity through Pectin methylesterase46‐modulated root cell wall pectin methylesterification in Arabidopsis. Plant Journal. 2017;90(3): 491–504. doi: 10.1111/tpj.13506 28181322

65. Claudio IB, Zed R, Miren A, María DLLM, Felipe A, Patricio AJ, et al. Molecular and physiological strategies to increase aluminum resistance in plants. Mol Biol Rep. 2012;39(3): 2069–2079. doi: 10.1007/s11033-011-0954-4 21660471

66. Korir PC, Zhang J, Wu K, Zhao T, Gai J. Association mapping combined with linkage analysis for aluminum tolerance among soybean cultivars released in Yellow and Changjiang River Valleys in China. Theor Appl Genet. 2013;126(6): 1659–1675. doi: 10.1007/s00122-013-2082-0 23515677

67. Zhang D, Li H, Wang J, Zhang H, Hu Z, Chu S, et al. High-density genetic mapping identifies new major loci for tolerance to low-phosphorus stress in soybean. Front Plant Sci. 2016;7(1086): 372.

68. López-Marín HD, Rao IM, Blair MW. Quantitative trait loci for root morphology traits under aluminum stress in common bean (Phaseolus vulgaris L.). Theor Appl Genet. 2009;119(3): 449–458. doi: 10.1007/s00122-009-1051-0 19436988

69. Teng W, Kang Y, Hou W, Hu H, Luo W, Wei J, et al. Phosphorus application reduces aluminum toxicity in two Eucalyptus clones by increasing its accumulation in roots and decreasing its content in leaves. PLoS One. 2018;13(1): e0190900. doi: 10.1371/journal.pone.0190900 29324770

70. Pandey GK, Grant JJ, Cheong YH, Kim BG, Li L, Luan S. ABR1, an APETALA2-domain transcription factor that functions as a repressor of ABA response in Arabidopsis. Plant Physiol. 2005;139(3): 1185–1193. doi: 10.1104/pp.105.066324 16227468

71. Hussain RM, Ali M, Feng X, Li X. The essence of NAC gene family to the cultivation of drought-resistant soybean (Glycine max L. Merr.) cultivars. BMC Plant Biol. 2017;17(1): 55. doi: 10.1186/s12870-017-1001-y 28241800

72. Xie ZM, Zou HF, Lei G, Wei W, Zhou QY, Niu CF, et al. Soybean trihelix transcription factors GmGT-2A and GmGT-2B improve plant tolerance to abiotic stresses in transgenic arabidopsis. PLoS One. 2009;4(9): e6898. doi: 10.1371/journal.pone.0006898 19730734

73. Inostrozablancheteau C, Rengel Z, Alberdi M, De lLMM, Aquea F, Arcejohnson P, et al. Molecular and physiological strategies to increase aluminum resistance in plants. Mol Bio Rep. 2012;39(3): 2069–2079.


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