Abstract
Aims
Longer root hair length (RHL) increases root surface area, thereby contributing to increased phosphorous uptake. This study aimed to identify useful germplasms and quantitative trait loci (QTL) for RHL improvement in wheat.
Methods
The genetic variation in RHL was examined using hydroponic culture in 117 hexaploid wheat strains. Rhizosheath size and phosphorous uptake ability were also examined using high P-fixing soils with extremely low phosphorous availability (Andisols). QTL analysis was performed using backcross inbred lines from a cross between a Spanish spelt strain and a bread wheat variety.
Results
A wide range in genetic variation was found, especially in spelt wheat and landraces of bread wheat, whereas modern bread wheat varieties tended to show shorter RHL. Interestingly, remarkably longer RHL were observed in Spanish spelt strains than in strains from other countries. RHL exhibited a significant positive correlation with rhizosheath size and phosphorous uptake in soils. A QTL on chromosome 2A (QRhl.obu-2A) conferring longer RHL by the allele of a Spanish spelt strain was identified. It was co-located with TaRSL4-2AS, a key regulator of root hair elongation.
Conclusions
Spanish spelt wheat strains could be unique germplasms that provide a useful allele for increasing RHL to enhance phosphorous uptake ability.
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Abbreviations
- P:
-
phosphorus
- RHL:
-
root hair length
- QTL:
-
quantitative trait loci
- SNP:
-
single nucleotide polymorphism
- BIL:
-
backcross inbred line
- SRL:
-
seminal root length
- PCR:
-
polymerase chain reaction
- SSR:
-
simple sequence repeat
- MQM:
-
multiple QTL model
- LOD:
-
logarithm of the odds
- PVE:
-
phenotypic variance explained
- ANOVA:
-
analysis of variance
References
Asakura N, Mori N, Nakamura C, Ohtsuka I (2009) Genotyping of the Q locus in wheat by a simple PCR-RFLP method. Genes Genet Syst 84:233–237
Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24:225–252. https://doi.org/10.1146/annurev.pp.24.060173.001301
Bilal HM, Aziz T, Maqsood MA, Farooq M, Yan G (2018) Categorization of wheat genotypes for phosphorus efficiency. PLoS One 13:e0205471. https://doi.org/10.1371/journal.pone.0205471
Brown LK, George TS, Dupuy LX, White PJ (2013) A conceptual model of root hair ideotypes for future agricultural environments: what combination of traits should be targeted to cope with limited P availability? Ann Bot 112:317–330. https://doi.org/10.1093/aob/mcs231
Caballero L, Martín LM, Alvarez JB (2006) Agrobiodiversity of hulled wheats in Asturias (north of Spain). Genet Resour Crop Ev 54:267–277. https://doi.org/10.1007/s10722-005-4049-8
Campbell KG (1997) Spelt: agronomy, genetics, and breeding. Plant Breed Rev 15:187–213. https://doi.org/10.1002/9780470650097.ch6
Cui S, Suzaki T, Tominaga-Wada R, Yoshida S (2018) Regulation and functional diversification of root hairs. Semin Cell Dev Biol 83:115–122. https://doi.org/10.1016/j.semcdb.2017.10.003
Delhaize E, James RA, Ryan PR (2012) Aluminium tolerance of root hairs underlies genotypic differences in rhizosheath size of wheat (Triticum aestivum) grown on acid soil. New Phytol 195:609–619. https://doi.org/10.1111/j.1469-8137.2012.04183.x
Delhaize E, Rathjen TM, Cavanagh CR (2015) The genetics of rhizosheath size in a multiparent mapping population of wheat. J Exp Bot 66:4527–4536. https://doi.org/10.1093/jxb/erv223
Department of Agriculture, Hokkaido (2015) Hokkaido Fertiliser recommendations 2015. Department of Agriculture, Hokkaido
de Souza Campos PM, Cornejo P, Rial C, Borie F, Varela RM, Seguel A, Lopez-Raez JA (2019) Phosphate acquisition efficiency in wheat is related to root:shoot ratio, strigolactone levels, and PHO2 regulation. J Exp Bot 70:5631–5642. https://doi.org/10.1093/jxb/erz349
Dolan L (2017) Root hair development in grasses and cereals (Poaceae). Curr Opin Genet Dev 45:76–81. https://doi.org/10.1016/j.gde.2017.03.009
Elía M, Moralejo M, Rodríguez-Quijano M, Molina-Cano JL (2004) Spanish spelt: a separate gene pool within the spelt germplasm. Plant Breed 123:297–299. https://doi.org/10.1111/j.1439-0523.2004.00969.x
Ellis H, Spielmeyer W, Gale R, Rebetzke J, Richards A (2002) "perfect" markers for the Rht-B1b and Rht-D1b dwarfing genes in wheat. Theor Appl Genet 105:1038–1042. https://doi.org/10.1007/s00122-002-1048-4
Gahoonia TS, Care D, Nielsen NE (1997) Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant Soil 191:181–188. https://doi.org/10.1023/a:1004270201418
George TS, Brown LK, Ramsay L, White PJ, Newton AC, Bengough AG, Russell J, Thomas WT (2014) Understanding the genetic control and physiological traits associated with rhizosheath production by barley (Hordeum vulgare). New Phytol 203:195–205. https://doi.org/10.1111/nph.12786
Gondwe RL, Kinoshita R, Sano M, Suminoe T, Aiuchi D, Koaze H, Palta J, Tani M (2017) Lack of yield response in potato (Solanum tuberosum L.) to phosphate fertilizer under contrasting soil types varying in phosphate absorption coefficient and available phosphate. Soil Sci Plant Nutr 63:171–177. https://doi.org/10.1080/00380768.2017.1282300
Guzman C, Caballero L, Martin LM, Alvarez JB (2012) Waxy genes from spelt wheat: new alleles for modern wheat breeding and new phylogenetic inferences about the origin of this species. Ann Bot 110:1161–1171. https://doi.org/10.1093/aob/mcs201
Haling RE, Brown LK, Bengough AG, Young IM, Hallett PD, White PJ, George TS (2013) Root hairs improve root penetration, root-soil contact, and phosphorus acquisition in soils of different strength. J Exp Bot 64:3711–3721. https://doi.org/10.1093/jxb/ert200
Han Y, Xin M, Huang K, Xu Y, Liu Z, Hu Z, Yao Y, Peng H, Ni Z, Sun Q (2016) Altered expression of TaRSL4 gene by genome interplay shapes root hair length in allopolyploid wheat. New Phytol 209:721–732. https://doi.org/10.1111/nph.13615
Heuer S, Gaxiola R, Schilling R, Herrera-Estrella L, Lopez-Arredondo D, Wissuwa M, Delhaize E, Rouached H (2017) Improving phosphorus use efficiency: a complex trait with emerging opportunities. Plant J 90:868–885. https://doi.org/10.1111/tpj.13423
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California agricultural Experimental Station circular 347. University of California, Berkeley
Horn R, Wingen LU, Snape JW, Dolan L (2016) Mapping of quantitative trait loci for root hair length in wheat identifies loci that co-locate with loci for yield components. J Exp Bot 67:4535–4543. https://doi.org/10.1093/jxb/erw228
International Wheat Genome Sequencing Consortium (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191. https://doi.org/10.1126/science.aar7191
Khabarov N, Obersteiner M (2017) Global phosphorus fertilizer market and national policies: a case study revisiting the 2008 price peak. Front Nutr 4:22. https://doi.org/10.3389/fnut.2017.00022
Kippes N, Debernardi JM, Vasquez-Gross HA, Akpinar BA, Budak H, Kato K, Chao S, Akhunov E, Dubcovsky J (2015) Identification of the VERNALIZATION 4 gene reveals the origin of spring growth habit in ancient wheats from South Asia. Proc Natl Acad Sci U S A 112:E5401–E5410. https://doi.org/10.1073/pnas.1514883112
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713. https://doi.org/10.1093/aob/mcl114
Liu M, Rathjen T, Weligama K, Forrest K, Hayden M, Delhaize E (2017) Analysis of aneuploid lines of bread wheat to map chromosomal locations of genes controlling root hair length. Ann Bot 119:1333–1341. https://doi.org/10.1093/aob/mcx030
Longin CFH, Wurschum T (2016) Back to the future - tapping into ancient grains for food diversity. Trends Plant Sci 21:731–737. https://doi.org/10.1016/j.tplants.2016.05.005
Matsuoka Y (2011) Evolution of polyploid Triticum wheats under cultivation: the role of domestication, natural hybridization and allopolyploid speciation in their diversification. Plant Cell Physiol 52:750–764. https://doi.org/10.1093/pcp/pcr018
Mew MC (2016) Phosphate rock costs, prices and resources interaction. Sci Total Environ 542:1008–1012. https://doi.org/10.1016/j.scitotenv.2015.08.045
Miguel MA, Postma JA, Lynch JP (2015) Phene synergism between root hair length and basal root growth angle for phosphorus acquisition. Plant Physiol 167:1430–1439. https://doi.org/10.1104/pp.15.00145
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36. https://doi.org/10.1016/S0003-2670(00)88444-5
Nestler J, Wissuwa M (2016) Superior root hair formation confers root efficiency in some, but not all, rice genotypes upon P deficiency. Front Plant Sci 7:1935. https://doi.org/10.3389/fpls.2016.01935
Pearse SJ, Veneklaas EJ, Cawthray G, Bolland MD, Lambers H (2007) Carboxylate composition of root exudates does not relate consistently to a crop species' ability to use phosphorus from aluminium, iron or calcium phosphate sources. New Phytol 173:181–190. https://doi.org/10.1111/j.1469-8137.2006.01897.x
Reif JC, Zhang P, Dreisigacker S, Warburton ML, van Ginkel M, Hoisington D, Bohn M, Melchinger AE (2005) Wheat genetic diversity trends during domestication and breeding. Theor Appl Genet 110:859–864. https://doi.org/10.1007/s00122-004-1881-8
Sakai Y, Cao L, Funata R, Shiraishi T, Yoshikawa K, Maeno K, Miura H, Onishi K (2018) QTLs for agronomic traits detected in recombinant inbred lines derived from a bread wheat x spelt cross. Breed Sci 68:587–595. https://doi.org/10.1270/jsbbs.18046
Simons KJ, Fellers JP, Trick HN, Zhang Z, Tai YS, Gill BS, Faris JD (2006) Molecular characterization of the major wheat domestication gene Q. Genetics 172:547–555. https://doi.org/10.1534/genetics.105.044727
Soil Survey Staff (2014) Key to soil taxonomy, Twelfth edn. USDA/NRCS, Washington D.C
Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. WH Freeman and Company, New York
Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114. https://doi.org/10.1007/s00122-004-1740-7
Stetter MG, Schmid K, Ludewig U (2015) Uncovering genes and ploidy involved in the high diversity in root hair density, length and response to local scarce phosphate in Arabidopsis thaliana. PLoS One 10:e0120604. https://doi.org/10.1371/journal.pone.0120604
Takenaka S, Nitta M, Nasuda S (2019) Population structure and association analyses of the core collection of hexaploid accessions conserved ex situ in the Japanese gene bank NBRP-wheat. Genes Genet Syst 93:237–254. https://doi.org/10.1266/ggs.18-00041
Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822. https://doi.org/10.1126/science.1183700
Truog E (1930) The determination of the readily available phosphorus of soils. J Am Soc Agro 22:874–882
van Ooijen JW (2002) MapQTL ® 6, software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma B.V, Wageningen
van Ooijen JW (2006) JoinMap ® 4, software for the calculation of genetic linkage maps in experimental population. Kyazma B.V, Wageningen
Vandamme E, Renkens M, Pypers P, Smolders E, Vanlauwe B, Merckx R (2013) Root hairs explain P uptake efficiency of soybean genotypes grown in a P-deficient Ferralsol. Plant Soil 369:269–282. https://doi.org/10.1007/s11104-012-1571-2
Voss-Fels KP, Qian L, Parra-Londono S, Uptmoor R, Frisch M, Keeble-Gagnere G, Appels R, Snowdon RJ (2017) Linkage drag constrains the roots of modern wheat. Plant Cell Environ 40:717–725. https://doi.org/10.1111/pce.12888
Wada K (1989) Allophane and Imogolite. In: Dixon JB, Weed SB (eds) Minerals in soil environments. SSSA, Madison, pp 1051–1087
Waines JG, Ehdaie B (2007) Domestication and crop physiology: roots of green-revolution wheat. Ann Bot 100:991–998. https://doi.org/10.1093/aob/mcm180
Wang W, Ding G-D, White PJ, Wang X-H, Jin K-M, Xu F-S, Shi L (2018) Mapping and cloning of quantitative trait loci for phosphorus efficiency in crops: opportunities and challenges. Plant Soil 439:91–112. https://doi.org/10.1007/s11104-018-3706-6
Wang Y, Thorup-Kristensen K, Jensen LS, Magid J (2016) Vigorous root growth is a better indicator of early nutrient uptake than root hair traits in spring wheat grown under low fertility. Front Plant Sci 7:865. https://doi.org/10.3389/fpls.2016.00865
Xie Q, Fernando KMC, Mayes S, Sparkes DL (2017) Identifying seedling root architectural traits associated with yield and yield components in wheat. Ann Bot 119:1115–1129. https://doi.org/10.1093/aob/mcx001
Xie Q, Mayes S, Sparkes DL (2015) Spelt as a genetic resource for yield component improvement in bread wheat. Crop Sci 55:2753–2765. https://doi.org/10.2135/cropsci2014.12.0842
Yan X, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265:17–29. https://doi.org/10.1007/s11104-005-0693-1
Yi K, Menand B, Bell E, Dolan L (2010) A basic helix-loop-helix transcription factor controls cell growth and size in root hairs. Nat Genet 42:264–267. https://doi.org/10.1038/ng.529
Zhang C, Simpson RJ, Kim CM, Warthmann N, Delhaize E, Dolan L, Byrne ME, Wu Y, Ryan PR (2018) Do longer root hairs improve phosphorus uptake? Testing the hypothesis with transgenic Brachypodium distachyon lines overexpressing endogenous RSL genes. New Phytol 217:1654–1666. https://doi.org/10.1111/nph.14980
Zhu J, Kaeppler SM, Lynch JP (2005) Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270:299–310. https://doi.org/10.1007/s11104-004-1697-y
Acknowledgements
We thank Ayumi Kadota, Ayaka Kinosita, and Mayumi Tokui for their assistance. We also thank Dr. Atsushi Torada, Dr. Kiyoaki Kato and two anonymous reviewers for their valuable comments on earlier version of this manuscript. This research was supported by the research program (Agro-Eco project), at the Obihiro University, Japan.
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Fig. S1
Response of RHL under three P levels (0, 10 and 100 μM) in hydroponic culture. Different letters indicate the significant difference between treatments in each strain (Tukey-Kramer test, P < 0.05). (PDF 171 kb)
Fig. S2
Relationships between variation in root hair length (RHL) and the origin of 117 strains in hexaploid wheat. Red circles: Spelt wheat, Open circles: Landraces of bread wheat, Green circles: Modern varieties of bread wheat. Number of strains evaluated was listed above the figure. * indicated macha wheat strain. (PDF 409 kb)
Fig. S3
Comparison of root hair traits between ‘Harukirari’ (A) and ‘KU-1025’ (B) grown in soils (Andisols). (PDF 185 kb)
Fig. S4
Frequency distribution of seminal root length (SRL) in BILs. Based on the mean value of each line (six replicates), the number of lines is represented incrementally in each SRL category by 0.5 cm. h2: broad-sense heritability. *** shows significance at the 0.1% level. (PDF 10 kb)
Fig. S5
A linkage map constructed using 188 molecular markers in BILs. (PDF 54 kb)
Fig. S6
Interaction between two QTLs for root hair length (RHL) on chromosomes 2A (QRhl.obu-2A) and 6B (QRhl.obu-6B). (A) Comparison of RHL among four classes of allele combinations of two QTLs. KU and Haru indicate ‘KU-1025’ and ‘Harukirari’ alleles, respectively. Alleles of QTLs were estimated by flanking markers (Xgwm448 for QRhl.obu-2A and Xgwm88 for QRhl.obu-6B). Error bars indicate standard deviation and the number of strains of each class is shown in parentheses. Different letters on bars indicate the significant differences among classes by Tukey-Kramer test (P < 0.05). (B) The result of two-way ANOVA. *** and * indicate significance at the 0.1 and 5% levels, respectively. ns indicates no significance. (PDF 134 kb)
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Okano, N., Goto, R., Kato, T. et al. Spanish spelt is unique germplasm for improvement of root hair length in hexaploid wheat. Plant Soil 452, 171–184 (2020). https://doi.org/10.1007/s11104-020-04555-8
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DOI: https://doi.org/10.1007/s11104-020-04555-8