Identification of Novel QTL Governing Root Architectural Traits in an Interspecific Soybean Population

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Manavalan, Lakshmi P ^a,f   Prince, Silvas J ^a   Musket, Theresa A ^a   Chaky, Julian ^b,e   Deshmukh, Rupesh ^a   Vuong, Tri D ^a   Song, Li ^a   Cregan, Perry B ^c   Nelson, James C ^d   Shannon, J Grover ^a   Specht, James E ^b   Nguyen, Henry T ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d KANSAS STATE UNIVERSITY   (United States)

^e PIONEER HI BRED INTERNATIONAL INC   (United States)

^f BAYER CROPSCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; PROTEIN AP2 EREBP; PROTEIN MYB; RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; BACKCROSSING; CHROMOSOME 8; GENETIC IDENTIFICATION; INBRED STRAIN; INTERSPECIFIC HYBRID; MORPHOLOGICAL TRAIT; NONHUMAN; PHENOTYPIC VARIATION; POPULATION BIOLOGY; PROTEIN EXPRESSION; QUANTITATIVE TRAIT LOCUS; RNA SEQUENCE; ROOT GROWTH; ROOT LENGTH; ROOT MORPHOLOGY; ROOT SYSTEM; SEEDLING; SHOOT GROWTH; SOYBEAN; SPECIES IDENTIFICATION; ANATOMY AND HISTOLOGY; EPISTASIS; GENETIC ASSOCIATION STUDY; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHENOTYPE; PLANT ROOT; SHOOT;

GLYCINE MAX;

EPISTASIS, GENETIC; GENETIC ASSOCIATION STUDIES; PHENOTYPE; PLANT ROOTS; PLANT SHOOTS; QUANTITATIVE TRAIT LOCI; SOYBEANS;

EID: 84924387903     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120490     Document Type: Article

References (83)

1. Tran LS, Mochida K. Functional genomics of soybean for improvement of productivity in adverse selection. Funct Integr Genomics 2010; 10: 447-62. doi: 10.1007/s10142-010-0178-z PMID: 20582712
2. Sinclair TR, Purcell LC, King CA, Sneller CH, Chen P, Vadez V, et al. Drought tolerance and yield increase of soybean resulting from improved symbiotic N fixation. Field Crops Res. 2007; 101: 68-71.
3. Price AH, Townend J, Jones MP, Audebert A, Courtois B. Mapping QTLs associated with drought avoidance in upland rice grown in the Philippines and West Africa. Plant Mol Biol. 2002; 48: 683-695. PMID: 11999843
4. Turner NC, Wright GC, Siddique KHM. Adaptation of grain legumes (pulses) to water limited environments. Adv Agron. 2001; 71: 193-223.
5. Abdel-Haleem H, Lee G, Boerma HR. Identification of QTL for increased fibrous roots in soybean. Theor Appl Genet. 2011; 122: 935-946. doi: 10.1007/s00122-010-1500-9 PMID: 21165732
6. Fenta BA, Schlüter U, Garcia BM, DuPlessis M, Foyer CH, Kunert KJ. Identification and Application of Phenotypic and Molecular Markers for Abiotic Stress Tolerance in Soybean. In: Krezhova D, editor. Soybean-Genetics and Novel Techniques for Yield Enhancement. InTech, Shanghai, China; 2011. pp. 181-200.
7. Nguyen HT, Babu RC, Blum A. Breeding for drought resistance in rice: physiology and molecular genetics considerations. Crop Sci. 1997; 37: 1426-1434.
8. Suji KK, Prince KSJ, Mankhar SP, Kanagaraj P, Poornima R, Amutha R, et al. Evaluation of rice near iso-genic lines with root QTLs for plant production and root traits in rainfed target populations of environment. Field Crops Res. 2012; 137: 89-96.
9. Tuberosa R, Salvi S, Giuliani S, Sanguineti MC, Frascaroli E, Conti S, et al. Genomics of root architecture and functions in maize. In: Costa de Oliveira A, Varshney RK, editors. Root genomics. Dordrecht, The Netherlands : Springer; 2011. pp. 179-204.
10. Wasson AP, Richards RA, Chatrath R, Misra SC, Prasad SVS, Rebetzke SS, et al. Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. J Exp Bot. 2012; 63: 3485-3498. doi: 10.1093/jxb/ers111 PMID: 22553286
11. Sponchiado BN, White JW, Castillo JA, Jones PG. Root growth of four common bean cultivars in relation to drought tolerance in environments with contrasting soil types. Exp Agric. 1987; 25:249-257.
12. Varshney RK, Pazhamala L, Kashiwagi J, Gaur PM, Krishnamurthy L, Hoisington D. Genomics and physiological approaches for root trait breeding to improve drought tolerance in chickpea (Cicer arietinum L.) In: Costa de Oliveira A, Varshney RK, editors. Root genomics. Dordrecht, The Netherlands : Springer; 2011. pp. 233-250.
13. Hufstetler EV, Boerma HR, Carter TE, Earl HG. Genotypic variation for three physiological traits affecting drought tolerance in soybean. Crop Sci. 2007; 47: 25-35.
14. Ha CV, Le DT, Nishiyama R, Watanabe Y, Tran UT, Dong NV, et al. Characterization of the newly developed soybean cultivar DT2008 in relation to the model variety W82 reveals a new genetic resource for comparative and functional genomics for improved drought tolerance. Bio Med Res Int. 2013; 759657. doi: 10.1155/2013/759657 PMID: 23509774
15. Matsuo N, Takahashi M, Fukami K, Tsuchiya S, Tasaka K. Root growth of two soybean cultivars grown under different groundwater level conditions. Plant Prod Sci. 2013; 16: 374-382.
16. Manavalan LP, Guttikonda SK, Tran LP, Nguyen HT. Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol. 2009; 50:1260-1276. doi: 10.1093/pcp/ pcp082 PMID: 19546148
17. Pantalone VR, Rebetzke GJ, Burton JW, Carter TE. Phenotypic evaluation of root traits in soybean and applicability to plant breeding. Crop Sci. 1996; 36:456-459.
18. Myers DB, Kitchen NR, Sudduth KA, Sharp RE, Miles RJ. Soybean root distribution related to claypan soil properties and apparent soil electrical conductivity. Crop Sci. 2007; 47:1498-1509.
19. Tanksley SD. Mapping polygenes. Annu Rev Genet. 1993; 27: 205-233. PMID: 8122902
20. Coudert Y, Périn C, Courtois B, Khong NG, Gantet P. Genetic control of root development in rice, the model cereal. Trends Plant Sci. 2010; 15: 219-226. doi: 10.1016/j.tplants.2010.01.008 PMID: 20153971
21. Manavalan LP, Guttikonda SK, Nguyen VT, Shannon JG, Nguyen HT. Evaluation of diverse soybean germplasm for root growth and architecture. Plant and Soil 2010; 330: 503-514.
22. Gizlice Z, Carter TE, Burton JW. Genetic base for North American public soybean cultivars released between 1947 and 1988. Crop Sci. 1994; 34: 1143-1151.
23. Kim KS, Bellendir S, Hudson KA, Hill CB, Hartman GL, Hyten DL, et al. Fine mapping the soybean aphid resistance gene Rag1 in soybean. Theor. Appl. Genet. 2010; 120: 1063-1071. doi: 10.1007/ s00122-009-1234-8 PMID: 20035316
24. Tanksley SD, McCouch SR. Seed banks and molecular maps: unlocking genetic potential from the wild. Science 1997; 277:1063-66. PMID: 9262467
25. Tanksley SD, Grandillo S, Fulton TM, Zamir D, Eshed Y, Petiard V, et al. Advanced backcross QTL analysis in a cross between an elite processing line of tomato and its wild relative L. pimpinellifolium. Theor Appl Genet. 1996; 92: 213-224. doi: 10.1007/BF00223378 PMID: 24166170
26. Xiao J, Li J, Grandillo S, Ahn SN, Yuan L, Tanksley SD, et al. Identification of trait-improving quantitative trait loci alleles from a wild rice relative, Orysa rufipogon. Genetics 1998; 150: 899-909. PMID: 9755218
27. Hartman GL, Wang TC, Hymowitz T. Sources of resistance to soybean rust in perennial Glycine species. Plant Dis. 1992; 76: 396-399.
28. Chen YY, Chen PY, de los Reyes BG. Differential responses of the cultivated and wild species of soybean to dehydration stress. Crop Sci. 2006; 46: 2041-2046.
29. Bauer S, Hymowitz T, Noel GR. Soybean cyst nematode resistance derived from Glycine tomentella in amphiploid (G. max × G. tomentella) hybrid lines. Nematropica 2007; 37: 277-285.
30. Lenis JM, Ellersieck M, Blevins DG, Sleper DA, Nguyen HT, Dunn D, et al. Differences in ion accumulation and salt tolerance among Glycine accessions. J Agron Crop Sci. 2011; 197: 302-310.
31. Kanamaru K, Wang S, Yamada T, Abe J, Kitamura K. Genetic analysis and biochemical characterization of the high lutein trait of wild soybean. Breed Sci. 2008; 58: 393-400.
32. Concibido VC, La Vallee B, Mclarid P, Pineda N, Meyer J, Hummel J, et al. Introgression of a quantitative trait locus for yield from Glycine soja into commercial soybean cultivars. Theor Appl Genet. 2003; 106: 575-582. PMID: 12595984
33. Li D, Pfeiffer TW, Cornelius PL. Soybean QTL for yield and yield components associated with Glycine soja alleles. Crop Sci. 2008; 48:571-581.
34. Wang D, Graef GL, Procopiuk AM, Diers BW. Identification of putative QTL that underlie yield in interspecific soybean backcross populations. Theor Appl Genet. 2004; 108: 458-46. PMID: 14504749
35. Carter TE, Nelson RL, Sneller CH, Cui Z. Genetic diversity in soybean. In: Specht JE Boerma HR editors. Soybeans: Improvement, Production, and Uses. Agronomy Monographs; 2004.pp. 301-416.
36. Tanksley SD, Nelson JC. Advanced backcross QTL analysis: A method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines. Theor Appl Genet. 1996; 92: 191-203. doi: 10.1007/BF00223376 PMID: 24166168
37. Grant D, Nelson RT, Cannon SB, Shoemaker RC. SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res. 2010; 38: D843-846. doi: 10.1093/nar/gkp798 PMID: 20008513
38. Prince SJ, Mutava RN, Pegoraro C, Oliveira ACD, Nguyen HT. Root characters In: Kole C editor. Genomics and Breeding for Climate Resilient Crops. Springer, Berlin, Germany; 2013. pp. 67-131.
39. Brensha W, Kantartzi SK, Meksem K, Grier RL, Barakat A, Lightfoot DA, et al. Genetic analysis of root and shoot traits in the 'Essex' by 'Forrest' recombinant inbred line population of soybean. J Pl Genom Sci. 2012; 1: 1-9.
40. Rong Z, Hai-Feng C, Xian-Zhi W, Bao-Duo W, Shui-Lian C, Xiao-juan Z, et al. Analysis of QTLs for Root Traits at Seedling Stage in Soybean. Acta Agron Sin. 2011; 37: 1151-1158.
41. Kabelka EA, Diers BW, Fehr W, LeRoy AR, Baianu IC, You T, et al. Putative alleles for increased yield from soybean plant introductions. Crop Sci. 2004; 44: 784-791.
42. Petrie CL, Hall AE. Water relations in cowpea and pearl millet under soil water deficits. II. Water use and root distribution. Aust J Plant Physiol. 1992; 19:591-600.
43. Hyten DL, Choi I, Song Q, Specht JE, Carter TE, Shoemaker RC, et al. A high density integrated genetic linkage map of soybean and the development of a 1536 universal soy linkage panel for quantitative trait locus mapping. Crop Sci. 2010; 50:960-968.
44. Li H, Ye G, Wang J. A modified algorithm for the improvement of composite interval mapping. Genetics 2007; 175: 361-374. PMID: 17110476
45. Joshi T, Patil K, Fitzpatrick MR, Franklin LD, Yao Q, Cook JR, et al. Soybean Knowledge Base (SoyKB): A Web resource for soybean translational genomics. BMC Genomics 2012; 13: 15. doi: 10. 1186/1471-2164-13-15 PMID: 22233149
46. Kim MY, Lee S, Van K, Kim TH, Jeong SC, Choi I, et al. Whole-genome sequencing and intensive analysis of the undomesticated soybean genome. Proc Natl Acad Sci. 2010; 107: 22032-22037. doi: 10. 1073/pnas.1009526107 PMID: 21131573
47. Lam HM, Xu X, Liu X, Chen W, Yang G, Wong F, et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat genet. 2010; 42: 1053-1059. doi: 10.1038/ng.715 PMID: 21076406
48. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, et al. GENEVESTIGATOR V3: a reference expression database for the meta-analysis of transcriptomes. Advances in Bioinformatics 2008; 420747. doi: 10.1155/2008/420747 PMID: 19956698
49. Severin AJ, Woody JL, Bolon Y, Joseph B, Diers BW, Farmer AD, et al. RNA seq atlas of Glycine max: A guide to the soybean transcriptome. BMC Plant Biol. 2010; 10:160. doi: 10.1186/1471-2229-10-160 PMID: 20687943
50. Livak K, Schmittgen T. Analysis of relative gene expression data using real-time quantitative PCR and the 2< sup>- ΔΔCT method. Methods 2001; 25: 402-408. PMID: 11846609
51. Rozen S, Skaletsky HJ. Primer3 on theWWWfor general users and for biologist programmers. In: Bioinformatics Methods and Protocols: Methods in Molecular Biology. Misener S, Krawetz SA, editors. Humana Press, Totowa, New Jersey; 2000. pp. 365-386.
52. Taylor HM, Burnett E, Booth GD. Tap root elongation rates of soybeans. J Agron and Crop Sci. 1978; 146: 33-39.
53. Cortes PM Sinclair TR. Water relations of field-grown soybean under drought. Crop Sci. 1986; 26: 993-998.
54. Liu Y, Gai JY, Lv HN. Identification of rhizosphere abiotic stress tolerance and related root traits in soybean. Acta Agron Sin. 2005; 31: 1132-1137.
55. Liu Y, Gai JY, Lv HN. Genetic variation of root traits at seedling stage and their relationship with stress tolerance in soybean. Soybean Sci. 2007; 26: 127-133.
56. Liang H, Yu Y, Yang H, Xu L,WDong, Du H, et al. Inheritance and QTL mapping of related root traits in soybean at the seedling stage. Theor Appl Genet. 2014; 127: 2127-2137. doi: 10.1007/s00122-014-2366-z PMID: 25145446
57. Lü CX, Guo JQ, Wang Y, Leng JT, Yang GM, Hou WS, et al. Identification, inheritance analysis and QTL mapping of root and shoot traits in soybean variety PI471938 with tolerance to wilting. Acta Agron Sin. 2010; 36: 1476-1483.
58. Alcivar A, Jacobson J, Rainho J, Meksem K, Lightfoot DA, Kassem MA. Genetic analysis of soybean plant height, hypocotyl and internode lengths. J Agric Food Environ Sci. 2007; 1: 1-20.
59. Sayama T, Nakazaki T, Ishikawa G, Yagasaki K, Yamada N, Hirota N et al. QTL analysis of seedflooding tolerance in soybean. Plant Sci. 2009; 176: 514-521.
60. Brucker E, Carlson S, Wright E, Niblack, T, Diers BW. Rhg1 alleles from soybean PI 437654 and PI
61. respond differentially to isolates of Heterodera glycines in the greenhouse. Theor Appl Genet. 2005; 111: 44-49. PMID: 15883792
62. Guo B, Sleper DA, Arelli PR, Shannon JG, Nguyen HT. Identification of QTLs associated with resistance to soybean cyst nematode races 2, 3 and 5 in soybean PI 90763. Theor Appl Genet. 2005; 111: 965-71. PMID: 16075207
63. Arahana VS, Graef GL, Specht JE, Steadman JR, Eskridge KM. Identification of QTLs for resistance to Sclerotinia sclerotiorum in soybean. Crop Sci. 2001; 41: 180-188.
64. Concibido VC, Diers BW, Arelli PR. A decade of QTL mapping for cyst nematode resistance in soybean. Crop Sci. 2004; 44: 1121-1131.
65. Weisemann JM, Matthews BF, Devine TE. Molecular markers located proximal to the soybean cyst nematode resistance gene, Rhg4. Theor Appl Genet. 1992; 85: 136-138. doi: 10.1007/BF00222850 PMID: 24197295
66. Liu S, Kandoth PK, Warren SD, Yeckel G, Heinz R, Alden J, et al. A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 2012; 492: 256-260. doi: 10.1038/nature11651 PMID: 23235880
67. Salas P, Oyarzo-Llaipen J, Wang D, Chase K, Mansur L. Genetic mapping of seed shape in three populations of recombinant inbred lines of soybean. Theor Appl Genet. 2006; 113:1459-1466. PMID: 17036219
68. Kim HK, Kang ST, Suh DY. Analysis of quantitative trait loci associated with leaflet types in two recombinant inbred lines of soybean Pl Breed. 2005; 124: 582-589.
69. Pooprompan P, Wasee S, Toojinda T, Abe J, Chanprame S, Srinives P. Molecular marker analysis of days to flowering in vegetable soybean. Kase J. 2006; 40: 573-581.
70. Hoeck JA, Fehr WR, Shoemaker RC, Welke GA, Johnson SL, Cianzio SR. Molecular marker analysis of seed size in soybean. Crop Sci. 2003; 43: 68-74.
71. Han Y, Li D, Zhu D, Li H, Li X, Teng W, et al. QTL analysis of soybean seed weight across multi-genetic backgrounds and environments. Theor Appl Genet. 2012; 125: 671-683. doi: 10.1007/s00122-012-1859-x PMID: 22481120
72. Reinprecht Y, Poysa VW, Yu KF, Rajcan I, Ablett GR, Pauls KP. Seed and agronomic QTL in low linolenic acid, lipoxygenase-free soybean germplasm. Genome 2006; 49: 1510-1527. PMID: 17426766
73. B Liu, Fujita T, Yan ZH, Sakamoto S, Xu D, Abe J. QTL mapping of domestication-related traits in soybean. Annals of Botany 2007; 100: 1027-1038. PMID: 17684023
74. Prince SJ, Song L, Qiu D, Santos JVMD, Chai C, Joshi T, et al. Genetic variants in root architecturerelated genes in a Glycine soja accession, a potential resource to improve cultivated soybean. BMC genomics 2015; 16: 132.
75. Du H, Yang S, Liang Z, Feng B, Liu L, Huang Y, et al. Genome wide analysis of MYB transcription factor superfamily in soybean. BMC Plant Biology 2012; 12: 106. doi: 10.1186/1471-2229-12-106 PMID: 22776508
76. Middleton PH, Jakab J, Penmetsa RV, Starker CG, Doll J, Kalo P, et al. An ERF transcription factor in Medicago trunculata that is essential for nod factor signal transduction. Plant Cell 2007; 19: 1221-1234. PMID: 17449807
77. Aharoni A, Dixit S, Jetter R, Thoenes E, Arkel GV, Pereira A. The SHINE clade of AP2 domain transcription factor activates wax biosynthesis, alters cuticle properties and confers drought tolerance when over expressed in Arabidopsis. Plant cell 2004; 16: 2463-2480. PMID: 15319479
78. Rodriguez-Uribe L, O'Connell MA. A root-specific bZIP transcription factor is responsive to water deficit stress in tepary bean and common bean. J Exp Bot. 2006; 57: 1391-1398. PMID: 16531461
79. Nishimura R, Ohmori M, Kawaguchi M. The novel symbiotic phenotype of enhanced nodulating mutant of Lotus japonicus: astray mutant is an early nodulating mutant with wider nodulation zone. Plant Cell Physiol. 2002; 43: 853-859. PMID: 12198187
80. Pantalone VR, Rebetzke GJ, Burton JW, Carter TE. Phenotypic evaluation of root traits in soybean and applicability to plant breeding. Crop Sci. 1996; 36:456-459.
81. Devi MJ, Sinclair TR. Nitrogen fixation drought tolerance of the slow-wilting soybean PI 471938. Crop Sci. 2013; 53: 2072-2078.
82. Chen P, Sneller CH, Purcell LC, Sinclair TR, King CA, Ishibashi T. Registration of soybean germplasm lines R01-416F and R01-581F for improved yield and nitrogen fixation under drought stress. J Plant Reg. 2007; 1:166-167.
83. Lauter ANM, Peiffer GA, Yin T, Whitham SA, Cook D, Shoemaker RC, et al. Identification of candidate genes involved in early iron deficiency chlorosis signaling in soybean roots and leaves. BMC Genomics 2014; 15: 702. doi: 10.1186/1471-2164-15-702 PMID: 25149281