Abstract
Main conclusion
Principal component and meta-QTL analyses identified genetic loci affecting the trade-off of wheat grain number and size, which could provide opportunities to optimize local breeding strategies for further yield improvement.
Abstract
Grain yield of wheat is complex, and its physiological and genetic bases remain largely unknown. Using the Forno/Oberkulmer recombinant inbred lines, this study validated the negative phenotypic relationships between thousand grain weight (TGW) and grain number components. This trade-off might be alleviated at the population level by early anthesis and at the shoot level by higher shoot biomass. Principal component (PC) analysis revealed three useful PCs, of which both PC1 and PC3 were positively associated with grain yield and grains m−2 through increased spikes m−2 (for PC1) or grains per spike (for PC3), while PC2 primarily reflected the trade-off of grain number and TGW. Quantitative trait locus (QTL) mapping detected eight and seven loci for PC1 and PC2, respectively, on chromosomes 1D, 2A, 3A, 3B, 4A, 4B, 5A and 7B, individually explaining 11.7‒29.3% of phenotypic variations. Using the 1203 QTLs published previously, a meta-analysis was performed to reveal 12, 21, 37 and 54 genomic regions (MQTLs) affecting grains m−2, spikes m−2, grains per spike and TGW, respectively. Moreover, 67 MQTLs (96%) for grain number were coincided with the TGW MQTLs, with reverse phenotypic effects, suggesting intensive genetic trade-off between grain number and size. The AGP2 gene, which encodes ADP-glucose pyrophosphorylase determining TGW, was found by haplotype analysis in the Forno/Oberkulmer population to affect grain number oppositely, indicating this trade-off at the gene level. Appropriate combinations of the QTLs/genes for local breeding targets, such as higher grain number or larger grains, therefore, would be critical to achieve future yield gains.
Similar content being viewed by others
Abbreviations
- CS:
-
Chinese Spring
- IWGSC:
-
International Wheat Genome Sequencing Consortium
- LOD:
-
Likelihood of odd
- MQTL:
-
Meta quantitative trait locus
- PC:
-
Principal component
- RIL:
-
Recombinant inbred line
- TGW:
-
Thousand grain weight
References
Bennett D, Izanloo A, Reynolds M, Kuchel H, Langridge P, Schnurbusch T (2012) Genetic dissection of grain yield and physical grain quality in bread wheat (Triticum aestivum L.) under water-limited environments. Theor Appl Genet 125:255–271
Börner A, Schumann E, Furste A, Coster H, Leithold B, Roder MS, Weber WE (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105:921–936
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Brinton J, Simmonds J, Minter F, Leverington-Waite M, Snape J, Uauy C (2017) Increased pericarp cell length underlies a major quantitative trait locus for grain weight in hexaploid wheat. New Phytol 215:1026–1038
Brocklehurst PA (1977) Factors controlling grain weight in wheat. Nature 266:348–349
Calderini DF, Abeledo LG, Savin R, Slafer GA (1999) Effect of temperature and carpel size during pre-anthesis on potential grain weight in wheat. J Agric Sci 132:453–459
Campbell KG, Bergman CJ, Gualberto DG, Anderson JA, Giroux MJ, Hareland G, Fulcher RG, Sorrells ME, Finney PL (1999) Quantitative trait loci associated with kernel traits in a soft × hard wheat cross. Crop Sci 39:1184–1195
Chairi F, Vergara-Diaz O, Vatter T, Aparicio N, Nieto-Taladriz MT, Kefauver SC, Bort J, Serret MD, Araus JL (2018) Post-green revolution genetic advance in durum wheat: the case of Spain. Field Crop Res 228:158–169
Deng Z, Cui Y, Han Q, Fang W, Li J, Tian J (2017) Discovery of consistent QTLs of wheat spike-related traits under nitrogen treatment at different development stages. Front Plant Sci 8:2120
Distelfeld A, Avni R, Fischer AM (2014) Senescence, nutrient remobilization, and yield in wheat and barley. J Exp Bot 65:3783–3798
Donald CM (1968) The breeding of crop ideotypes. Euphytica 17:385–403
Dreccer MF, van Herwaarden AF, Chapman SC (2009) Grain number and grain weight in wheat lines contrasting for stem water soluble carbohydrate concentration. Field Crop Res 112:43–54
Gambín BL, Borrás L (2010) Resource distribution and the trade-off between seed number and seed weight: a comparison across crop species. Ann Appl Biol 156:91–102
Gegas VC, Nazari A, Griffiths S, Simmonds J, Fish L, Orford S, Sayers L, Doonan JH, Snape JW (2010) A genetic framework for grain size and shape variation in wheat. Plant Cell 22:1046–1056
Golan G, Ayalon I, Perry A, Zimran G, Ade-Ajayi T, Mosquna A, Distelfeld A, Peleg Z (2019) GNI-A1 mediates trade-off between grain number and grain weight in tetraploid wheat. Theor Appl Genet 132:2353–2365
González FG, Miralles DJ, Slafer GA (2011) Wheat floret survival as related to pre-anthesis spike growth. J Exp Bot 62:4889–4901
Griffiths S, Wingen L, Pietragalla J, Garcia G, Hasan A, Miralles D, Calderini DF, Ankleshwaria JB, Waite ML, Simmonds J, Snape J, Reynolds M (2015) Genetic dissection of grain size and grain number trade-offs in CIMMYT wheat germplasm. PLoS ONE 10:e0118847
Guan P, Lu L, Jia L, Kabir MR, Zhang J, Lan T, Zhao Y, Xin M, Hu Z, Yao Y, Ni Z, Sun Q, Peng H (2018) Global QTL analysis identifies genomic regions on chromosomes 4A and 4B harboring stable loci for yield-related traits across different environments in wheat (Triticum aestivum L.). Front Plant Sci 9:529
Hasan AK, Herrera J, Lizana C, Calderini DF (2011) Carpel weight, grain length and stabilized grain water content are physiological drivers of grain weight determination of wheat. Field Crop Res 123:241–247
Hou J, Li T, Wang Y, Hao C, Liu H, Zhang X (2017) ADP-glucose pyrophosphorylase genes, associated with kernel weight, underwent selection during wheat domestication and breeding. Plant Biotechnol J 15:1533–1543
IWGSC (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191
Ji X, Shiran B, Wan J, Lewis DC, Jenkins CLD, Condon AG, Richards RA, Dolferus R (2010) Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant Cell Environ 33:926–942
Jia H, Wan H, Yang S, Zhang Z, Kong Z, Xue S, Zhang L, Ma Z (2013) Genetic dissection of yield-related traits in a recombinant inbred line population created using a key breeding parent in China’s wheat breeding. Theor Appl Genet 126:2123–2139
Jiang Y, Jiang Q, Hao C, Hou J, Wang L, Zhang H, Zhang S, Chen X, Zhang X (2015) A yield-associated gene TaCWI, in wheat: its function, selection and evolution in global breeding revealed by haplotype analysis. Theor Appl Genet 128:131–143
Kirby EJM (1988) Analysis of leaf, stem and ear growth in wheat from terminal spikelet stage to anthesis. Field Crop Res 18:127–140
Kuchel H, Williams KJ, Langridge P, Eagles HA, Jefferies SP (2007) Genetic dissection of grain yield in bread wheat. I QTL Analysis Theor Appl Genet 115:1029–1041
Labra MH, Struik PC, Evers JB, Calderini DF (2017) Plasticity of seed weight compensates reductions in seed number of oilseed rape in response to shading at flowering. Eur J Agron 84:113–124
Lalonde S, Morse D, Saini HS (1997) Expression of a wheat ADP-glucose pyrophosphorylase gene during development of normal and water-stress-affected anthers. Plant Mol Biol 34:445–453
Lee S, Eom J, Hwang S, Shin D, An G, Okita TW, Jeon J (2016) Plastidic phosphoglucomutase and ADP-glucose pyrophosphorylase mutants impair starch synthesis in rice pollen grains and cause male sterility. J Exp Bot 67:5557–5569
Li F, Wen W, He Z, Liu J, Jin H, Cao S, Geng H, Yan J, Zhang P, Wan Y, Xia X (2018) Genome-wide linkage mapping of yield-related traits in three Chinese bread wheat populations using high-density SNP markers. Theor Appl Genet 131:1903–1924
Liu Y, Lin Y, Gao S, Li Z, Ma J, Deng M, Chen G, Wei Y, Zheng Y (2017a) A genome-wide association study of 23 agronomic traits in Chinese wheat landraces. Plant J 91:861–873
Liu Y, Zhang J, Hu Y, Chen J (2017b) Dwarfing genes Rht4 and Rht-B1b affect plant height and key agronomic traits in common wheat under two water regimes. Field Crop Res 204:242–248
Liu K, Sun X, Ning T, Duan X, Wang Q, Liu T, An Y, Guan X, Tian J, Chen J (2018) Genetic dissection of wheat panicle traits using linkage analysis and a genome-wide association study. Theor Appl Genet 131:1073–1090
Lizana XC, Riegel R, Gomez LD, Herrera J, Isla A, McQueen-Mason SJ, Calderini DF (2010) Expansins expression is associated with grain size dynamics in wheat (Triticum aestivum L.). J Exp Bot 61:1147–1157
Lo Valvo PJ, Miralles DJ, Serrago RA (2018) Genetic progress in Argentine bread wheat varieties released between 1918 and 2011: changes in physiological and numerical yield components. Field Crop Res 221:314–321
Lozada DN, Mason RE, Sukumaran S, Dreisigacker S (2018) Validation of grain yield QTLs from soft winter wheat using a CIMMYT spring wheat panel. Crop Sci 58:1964–1971
Ma Z, Sorrells ME (1995) Genetic analysis of fertility restoration in wheat using restriction fragment length polymorphisms. Crop Sci 35:1137–1143
Maccaferri M, Sanguineti MC, Demontis A, El-Ahmed A, del Moral LG, Maalouf F, Nachit M, Nserallah N, Ouabbou H, Rhouma S, Royo C, Villegas D, Tuberosa R (2011) Association mapping in durum wheat grown across a broad range of water regimes. J Exp Bot 62:409–438
Maphosa L, Langridge P, Taylor H, Parent B, Emebiri LC, Kuchel H, Reynolds MP, Chalmers KJ, Okada A, Edwards J, Mather DE (2014) Genetic control of grain yield and grain physical characteristics in a bread wheat population grown under a range of environmental conditions. Theor Appl Genet 127:1607–1624
Maydup ML, Antonietta M, Guiamet JJ, Graciano C, López JR, Tambussi EA (2010) The contribution of ear photosynthesis to grain filling in bread wheat (Triticum aestivum L.). Field Crop Res 119:48–58
McIntyre CL, Mathews KL, Rattey A, Chapman SC, Drenth J, Ghaderi M, Reynolds M, Shorter R (2010) Molecular detection of genomic regions associated with grain yield and yield-related components in an elite bread wheat cross evaluated under irrigated and rainfed conditions. Theor Appl Genet 120:527–541
Messmer MM, Keller M, Zanetti S, Keller B (1999) Genetic linkage map of a wheat × spelt cross. Theor Appl Genet 98:1163–1170
Qin X, Zhang F, Liu C, Yu H, Cao B, Tian S, Liao Y, Siddique KHM (2015) Wheat yield improvements in China: past trends and future directions. Field Crop Res 177:117–124
Quarrie SA, Quarrie SP, Radosevic R, Rancic D, Kaminska A, Barnes JD, Leverington M, Ceoloni C, Dodig D (2006) Dissecting a wheat QTL for yield present in a range of environments: from the QTL to candidate genes. J Exp Bot 57:2627–2637
Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS ONE 8:e66428
Rebetzke GJ, van Herwaarden AF, Jenkins C, Weiss M, Lewis D, Ruuska S, Tabe L, Fettell NA, Richards RA (2008) Quantitative trait loci for water-soluble carbohydrates and associations with agronomic traits in wheat. Aust J Agric Res 59:891–905
Rebetzke GJ, Bonnett DG, Reynolds MP (2016) Awns reduce grain number to increase grain size and harvestable yield in irrigated and rainfed spring wheat. J Exp Bot 67:2573–2586
Reynolds M, Foulkes J, Furbank R, Griffiths S, King J, Murchie E, Parry M, Slafer G (2012) Achieving yield gains in wheat. Plant Cell Environ 35:1799–1823
Sadras VO (2007) Evolutionary aspects of the trade-off between seed size and number in crops. Field Crop Res 100:125–138
Sadras VO, Denison RF (2009) Do plant parts compete for resources? An evolutionary viewpoint. New Phytol 183:565–574
Sanchez-Bragado R, Molero G, Reynolds MP, Araus JL (2014) Relative contribution of shoot and ear photosynthesis to grain filling in wheat under good agronomical conditions assessed by differential organ δ13C. J Exp Bot 65:5401–5413
Sanchez-Bragado R, Kim JW, Rivera-Amado C, Molero G, Araus JL, Savin R, Slafer GA (2020) Are awns truly relevant for wheat yields? A study of performance of awned/awnless isogenic lines and their response to source–sink manipulations. Field Crop Res 254:107827
Sanchez-Garcia M, Royo C, Aparicio N, Martin-Sanchez JA, Alvaro F (2013) Genetic improvement of bread wheat yield and associated traits in Spain during the 20th century. J Agric Sci 151:105–118
Schulthess AW, Reif JC, Ling J, Plieske J, Kollers S, Ebmeyer E, Korzun V, Argillier O, Stiewe G, Ganal MW, Röder MS, Jiang Y (2017) The roles of pleiotropy and close linkage as revealed by association mapping of yield and correlated traits of wheat (Triticum aestivum L.). J Exp Bot 68:4089–4101
Shearman VJ, Sylvester-Bradley R, Scott RK, Foulkes MJ (2005) Physiological processes associated with wheat yield progress in the UK. Crop Sci 45:175–185
Shi S, Azam FI, Li H, Chang X, Li B, Jing R (2017) Mapping QTL for stay-green and agronomic traits in wheat under diverse water regimes. Euphytica 213:246
Slafer GA (2012) Wheat development: its role in phenotyping and improving crop adaptation. In: Reynolds MP, Pask AJD, Mullan DM (eds) Physiological breeding I: interdisciplinary approaches to improve crop adaptation. CIMMYT, Mexico, pp 107–121
Slafer GA, Savin R, Sadras VO (2014) Coarse and fine regulation of wheat yield components in response to genotype and environment. Field Crop Res 157:71–83
Sukumaran S, Dreisigacker S, Lopes M, Chavez P, Reynolds MP (2015) Genome-wide association study for grain yield and related traits in an elite spring wheat population grown in temperate irrigated environments. Theor Appl Genet 128:353–363
Sukumaran S, Lopes M, Dreisigacker S, Reynolds M (2018) Genetic analysis of multi-environmental spring wheat trials identifies genomic regions for locus-specific trade-offs for grain weight and grain number. Theor Appl Genet 131:985–998
Sylvester-Bradley R, Berry P, Blake J, Kindred D, Spink J, Bingham I, McVittie J, Foulkes J (2008) The wheat growth guide, 2nd edn. HGCA, London
Thorneycroft D, Hosein F, Thangavelu M, Clark J, Vizir I, Burrell MM, Ainsworth C (2003) Characterization of a gene from chromosome 1B encoding the large subunit of ADPglucose pyrophosphorylase from wheat: evolutionary divergence and differential expression of Agp2 genes between leaves and developing endosperm. Plant Biotechnol J 1:259–270
Tottman DR, Broad H (1987) The decimal code for the growth stages of cereals, with illustrations. Ann Appl Biol 110:441–454
van Herwaarden AF, Angus JF, Richards RA, Farquhar GD (1998) ‘Haying-off’, the negative grain yield response of dryland wheat to nitrogen fertiliser. II. Carbohydrate and protein dynamics. Aust J Agric Res 49:1083–1093
Van Ooijen JW (2009) MapQTL® 6, software for the mapping of quantitative traits loci in experimental populations of diploid species. Wageningen, Kyazma BV
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, IWGSC, Lillemo M, Mather D, Appels R, Dolferus R, Brown-Guedira G, Korol A, Akhunova AR, Feuillet C, Salse J, Morgante M, Pozniak C, Luo M, Dvorak J, Morell M, Dubcovsky J, Ganal M, Tuberosa R, Lawley C, Mikoulitch I, Cavanagh C, Edwards KJ, Hayden M, Akhunov E (2014) Characterization of polyploid wheat genomic diversity using a high-density 90 000 single nucleotide polymorphism array. Plant Biotechnol J 12:787–796
Xie Q, Mayes S, Sparkes DL (2015) Carpel size, grain filling, and morphology determine individual grain weight in wheat. J Exp Bot 66:6715–6730
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
Xie Q, Li N, Yang Y, Lv Y, Yao H, Wei R, Sparkes DL, Ma Z (2018) Pleiotropic effects of the wheat domestication gene Q on yield and grain morphology. Planta 247:1089–1098
Xu Y, Li S, Li L, Ma F, Fu X, Shi Z, Xu H, Ma P, An D (2017) QTL mapping for yield and photosynthetic related traits under different water regimes in wheat. Mol Breed 37:34
Yang J, Zhou Y, Wu Q, Chen Y, Zhang P, Zhang Ye HuW, Wang X, Zhao H, Dong L, Han J, Liu Z, Cao T (2019) Molecular characterization of a novel TaGL3-5A allele and its association with grain length in wheat (Triticum aestivum L.). Theor Appl Genet 132:1799–1814
Zhai H, Feng Z, Du X, Song Y, Liu X, Qi Z, Song L, Li J, Li L, Peng H, Hu Z, Yao Y, Xin M, Xiao S, Sun Q, Ni Z (2018) A novel allele of TaGW2-A1 is located in a finely mapped QTL that increases grain weight but decreases grain number in wheat (Triticum aestivum L.). Theor Appl Genet 131:539–553
Acknowledgements
We thank Beat Keller (University of Zurich, Switzerland) and Monika Messmer (Research Institute of Organic Agriculture, Switzerland) for providing the plant materials and marker information of the Forno/Oberkulmer RIL population. This work was supported by the Natural Science Foundation of China (No.: 31801354) and the Innovation and Entrepreneurship Talents Program of Jiangsu, China.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xie, Q., Sparkes, D.L. Dissecting the trade-off of grain number and size in wheat. Planta 254, 3 (2021). https://doi.org/10.1007/s00425-021-03658-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-021-03658-5