Abstract
Inflorescence structure affects final grain yield (GY) in wheat (Triticum aestivum L.). Recent breeding efforts have focused on improving grain number per spike, which is positively correlated with GY. Grain Number Increase 1 (GNI-A1) encodes a homeodomain leucine zipper class I (HD-Zip I) transcription factor that controls the number of grains per spike and GY. However, how this increase in grain number affects grain quality, especially grain protein content (GPC) in wheat, remains elusive. Here we investigated within-spikelet variation in GPC using GNI-A1 near-isogenic lines. Yield trials in two seasons and at two sites demonstrated that lines harboring a reduced-function allele, GNI-A1 (105Y), consistently showed improved GY due to a 27% increase in grain number per spike, along with a 1.7% reduction in GPC compared with lines containing a functional allele, GNI-A1 (105N). We confirmed the positive correlation between GY and grain number and the negative correlation between GY and GPC, but we observed no correlation between GY and thousand-grain weight. The increased grain number conferred by the 105Y allele was due to better floret fertility around the central part of the spike and whole florets. In-depth phenotypic analysis using dissected grain samples revealed that GPC was nearly uniform among spikelets and florets. These results suggest that in plants carrying a mutation in GNI-A1, the increase in the total number of grains is accompanied by a reduction in GPC.
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References
Asseng S, Milroy SP (2006) Simulation of environmental and genetic effects on grain protein concentration in wheat. Eur J Agron 25(2):119–128. https://doi.org/10.1016/j.eja.2006.04.005
Cullis BR, Smith AB, Coombes NE (2006) On the design of early generation variety trials with correlated data. J Agric Biol Environ Stat 11(4):381–393. https://doi.org/10.1198/108571106X154443
Debaeke P, Aussenac T, Fabre JL, Hilaire A, Pujol B, Thuries L (1996) Grain nitrogen content of winter bread wheat (Triticum aestivum L.) as related to crop management and to the previous crop. Eur J Agron 5(3):273–286. https://doi.org/10.1016/S1161-0301(96)02038-2
Dixon LE, Pasquariello M, Badgami R, Levin KA, Poschet G, Ng PQ, Orford S, Chayut N, Adamski NM, Brinton J, Simmonds J, Steuernagel B, Searle IR, Uauy C, Boden SA (2022) MicroRNA-resistant alleles of HOMEOBOX DOMAIN-2 modify inflorescence branching and increase grain protein content of wheat. Sci Adv 8(19):5907. https://doi.org/10.1126/sciadv.abn5907
Farrer DC, Weisz R, Heiniger R, Murphy JP, White JG (2006) Minimizing protein variability in soft red winter wheat: impact of nitrogen application timing and rate. Agron J 98(4):1137–1145. https://doi.org/10.2134/agronj2006.0039
Fischer RA, Howe GN, Ibrahim Z (1993) Irrigated spring wheat and timing and amount of nitrogen fertilizer. I. Grain yield and protein content. Field Crops Res 33(1):37–56. https://doi.org/10.1016/0378-4290(93)90093-3
Fujihara S, Sasaki H, Aoyagi Y, Sugahara T (2008) Nitrogen-to-protein conversion factors for some cereal products in Japan. J Food Sci 73(3):C204-209. https://doi.org/10.1111/j.1750-3841.2008.00665.x
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(8):2353–2365. https://doi.org/10.1007/s00122-019-03358-5
Groos C, Robert N, Bervas E, Charmet G (2003) Genetic analysis of grain protein-content, grain yield and thousand-kernel weight in bread wheat. Theor Appl Genet 106(6):1032–1040. https://doi.org/10.1007/s00122-002-1111-1
Kartseva T, Alqudah AM, Aleksandrov V, Alomari DZ, Doneva D, Arif MAR, Borner A, Misheva S (2023) Nutritional genomic approach for improving grain protein content in wheat. Foods 12(7):1399. https://doi.org/10.3390/foods12071399
Kramer T (1979) Environmental and genetic variation for protein content in winter wheat (Triticum aestivum L.). Euphytica 28(2):209–218. https://doi.org/10.1007/BF00056577
Li S, Tian Y, Wu K, Ye Y, Yu J, Zhang J, Liu Q, Hu M, Li H, Tong Y, Harberd NP, Fu X (2018) Modulating plant growth-metabolism coordination for sustainable agriculture. Nature 560(7720):595–600. https://doi.org/10.1038/s41586-018-0415-5
Pan Y, Han X, Xu H, Wu W, Liu X, Li Y, Xue C (2023) Elevated atmospheric CO(2) delays the key timing for split N applications to improve wheat (Triticum aestivum L.) protein composition. Front Plant Sci 14:1186890. https://doi.org/10.3389/fpls.2023.1186890
Sakuma S, Koppolu R (2023) Form follows function in Triticeae inflorescences. Breed Sci 73(1):46–56. https://doi.org/10.1270/jsbbs.22085
Sakuma S, Schnurbusch T (2020) Of floral fortune: tinkering with the grain yield potential of cereal crops. New Phytol 225(5):1873–1882. https://doi.org/10.1111/nph.16189
Sakuma S, Golan G, Guo Z, Ogawa T, Tagiri A, Sugimoto K, Bernhardt N, Brassac J, Mascher M, Hensel G, Ohnishi S, Jinno H, Yamashita Y, Ayalon I, Peleg Z, Schnurbusch T, Komatsuda T (2019) Unleashing floret fertility in wheat through the mutation of a homeobox gene. Proc Natl Acad Sci USA 116(11):5182. https://doi.org/10.1073/pnas.1815465116
Tanabata T, Shibaya T, Hori K, Ebana K, Yano M (2012) SmartGrain: high-throughput phenotyping software for measuring seed shape through image analysis. Plant Physiol 160(4):1871–1880. https://doi.org/10.1104/pp.112.205120
Terasawa Y, Ito M, Tabiki T, Nagasawa K, Hatta K, Nishio Z (2016) Mapping of a major QTL associated with protein content on chromosome 2B in hard red winter wheat (Triticum aestivum L.). Breed Sci 66(4):471–480. https://doi.org/10.1270/jsbbs.16026
Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC Gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314(5803):1298–1301. https://doi.org/10.1126/science.1133649
Acknowledgements
We would like to thank Masako Iwashita (Arid Land Research Center, Tottori University) for her help and support with phenotyping. We also thank Izzat Sidahmed Ali Tahir (Agricultural Research Corporation, Sudan) and Hongjing Zhu (Tottori University) for their valuable comments.
Funding
This research was financially supported by Grant-in-Aid for Young Scientists (B) 16K18635 (to S.S.) and Grant-in-Aid for Scientific Research (B) 22H02312 (to S.S.).
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S.S. and H.T. designed research. N.R., S.O., H.J., and Y.Y. performed phenotyping and data collection. S.S. and N.R. analyzed data. The first draft of the manuscript was written by S.S. and H.T. All authors read and approved the final manuscript.
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Sakuma, S., Rokuhara, N., Ohnishi, S. et al. Mutation of the wheat homeobox gene Grain Number Increase 1 increases grain number and grain yield but decreases grain protein content. Euphytica 220, 64 (2024). https://doi.org/10.1007/s10681-024-03327-0
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DOI: https://doi.org/10.1007/s10681-024-03327-0