Genome-wide association mapping and candidate genes analysis of high-throughput image descriptors for wheat frost tolerance

Abstract

Repeated occurrences of extreme weather events, such as low temperatures, due to global warming present a serious risk to the safety of wheat production. Quantitative assessment of frost damage can facilitate the analysis of key genetic factors related to wheat tolerance to abiotic stress. We collected 491 wheat accessions and selected four image-based descriptors (BLUE band, RED band, NDVI, and GNDVI) to quantitatively assess their frost damage. Image descriptors can complement the visual estimation of frost damage. Combined with genome-wide association study (GWAS), a total of 107 quantitative trait loci (QTL) (r² ranging from 0.75% to 9.48%) were identified, including the well-known frost-resistant locus Frost Resistance (FR)-A1/ Vernalization (VRN)-A1. Additionally, through quantitative gene expression data and mutation experience verification experiments, we identified two other frost tolerance candidate genes TraesCS2A03G1077800 and TraesCS5B03G1008500. Furthermore, when combined with genomic selection (GS), image-based descriptors can predict frost damage with high accuracy (r ≤ 0.84). In conclusion, our research confirms the accuracy of image-based high-throughput acquisition of frost damage, thereby supplementing the exploration of the genetic structure of frost tolerance in wheat within complex field environments.

Keywords

Wheat / Frost / Image / GWAS (genome-wide association study) / GS (genomic selection)

References

[1] Araus JL, Kefauver SC, Zaman-Allah M, et al. . Translating high-throughput phenotyping into genetic gain. Trends Plant Sci, 2018, 23: 451-466.

[2] Arshad S, Kazmi JH, Javed MG, et al. . Applicability of machine learning techniques in predicting wheat yield based on remote sensing and climate data in Pakistan, South Asia. Euro J Agronomy, 2023, 147: 126837.

[3] Babben S, Schliephake E, Janitza P, et al. . Association genetics studies on frost tolerance in wheat (Triticum aestivum L.) reveal new highly conserved amino acid substitutions in CBF-A3, CBF-A15, VRN3 and PPD1 genes. BMC Genomics, 2018, 19: 409

[4] Bates D, Mächler M, Bolker BM, et al. . lme4: Linear mixed-effects models using Eigen and S4. R Package Version, 2015, 1: 1.

[5] Botstein D, White RL, Skolnick M, et al. . Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet, 1980, 32: 314-331. DOI:

[6] Broge NH, Leblanc E. Comparing prediction power and stability of broadband and hyperspectral vegetation indices for estimation of green leaf area index and canopy chlorophyll density. Remote Sens Environ, 2001, 76: 156-172.

[7] Burgueño J, Crossa J, Rodríguez F, Yeater KM (2018) Augmented designs-experimental designs in which all treatments are not replicated. In: Glaz B, Yeater KM (eds) Applied Statistics in Agricultural, Biological, and Environmental Sciences. https://doi.org/10.2134/appliedstatistics.2016.0005.c13

[8] Chen Y, Sidhu HS, Kaviani M, et al. . Application of image-based phenotyping tools to identify QTL for in-field winter survival of winter wheat ( Triticum aestivum L.). Theor Appl Genet, 2019, 132: 2591-2604.

[9] Michaels SD, Amasino RM, et al. . Flowering locus C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell, 1999, 11(5): 949-956.

[10] Dhillon T, Pearce SP, Stockinger EJ, et al. . Regulation of Freezing Tolerance and Flowering in Temperate Cereals: The VRN-1 Connection. Plant Physiol, 2010, 153: 1846-1858.

[11] Endelman JB. Ridge regression and other kernels for genomic selection with R package rrBLUP. The Plant Genome, 2011, 4: 250-255.

[12] Furbank RT, Tester M. Phenomics – technologies to relieve the phenotyping bottleneck. Trends Plant Sci, 2011, 16: 635-644.

[13] Galiba G, Quarrie SA, Sutka J, et al. . RFLP mapping of the vernalization ( Vrn1 ) and frost resistance ( Fr1 ) genes on chromosome 5A of wheat. Theor Appl Genet, 1995, 90: 1174-1179.

[14] Galiba G, Vágújfalvi A, Li C, et al. . Regulatory genes involved in the determination of frost tolerance in temperate cereals. Plant Sci, 2009, 176: 12-19.

[15] Gao J, Hu X, Gao C, et al. . Deciphering genetic basis of developmental and agronomic traits by integrating high-throughput optical phenotyping and genome-wide association studies in wheat. Plant Biotechnol J, 2023, 21: 1966-1977.

[16] Gitelson AA, Kaufman YJ, Merzlyak MN. Use of a green channel in remote sensing of global vegetation from EOS-MODIS. Remote Sens Environ, 1996, 58: 289-298.

[17] Gobbett DL, Nidumolu U, Jin H, et al. . Minimum temperature mapping augments Australian grain farmers’ knowledge of frost. Agricul Forest Meteorol, 2021, 304–305108422

[18] Guo X, Liu D, Chong K. Cold signaling in plants: Insights into mechanisms and regulation. J Integr Plant Biol, 2018, 60: 745-756.

[19] Hassan MA, Xiang C, Farooq M, et al. . Cold stress in wheat: plant acclimation responses and management strategies. Front Plant Sci, 2021, 12676884

[20] Hennessy A, Clarke K, Lewis M. Hyperspectral classification of plants: A review of waveband selection generalisability. Remote Sensing, 2020, 12113

[21] Hyles J, Bloomfield MT, Hunt JR, et al. . Phenology and related traits for wheat adaptation. Heredity, 2020, 125: 417-430.

[22] Kidokoro S, Shinozaki K, Yamaguchi-Shinozaki K. Transcriptional regulatory network of plant cold-stress responses. Trends Plant Sci, 2022, 27: 922-935.

[23] Kobayashi F, Takumi S, Kume S, et al. . Regulation by Vrn-1/Fr-1 chromosomal intervals of CBF-mediated Cor/Lea gene expression and freezing tolerance in common wheat. J Exp Bot, 2005, 56: 887-895.

[24] Li MX, Yeung JM, Cherny SS, et al. . Evaluating the effective numbers of independent tests and significant p-value thresholds in commercial genotyping arrays and public imputation reference datasets. Hum Genet, 2012, 131: 747-756.

[25] Li Q, Zheng Q, Shen W, et al. . Understanding the biochemical basis of temperature-induced lipid pathway adjustments in plants. Plant Cell, 2015, 27: 86-103.

[26] Li H, Feng H, Guo C, et al. . High-throughput phenotyping accelerates the dissection of the dynamic genetic architecture of plant growth and yield improvement in rapeseed. Plant Biotechnol J, 2020, 18: 2345-2353.

[27] Li RX, Jin XL, Hu XJ et al (2019) Physiological responses and differential expression of cold resistance-related genes of six varieties of Magnoliaceae under low temperature stress. Acta Ecologica Sinica 39(8):2883–98. Verification. https://doi.org/10.5846/stxb201801230185

[28] Liu Y, Dang P, Liu L, et al. . Cold acclimation by the CBF–COR pathway in a changing climate: Lessons from Arabidopsis thaliana. Plant Cell Rep, 2019, 38: 511-519.

[29] Maccioni A, Agati G, Mazzinghi P. New vegetation indices for remote measurement of chlorophylls based on leaf directional reflectance spectra. J Photochem Photobiol, B, 2001, 61: 52-61.

[30] Martino DL, Abbate PE. Frost damage on grain number in wheat at different spike developmental stages and its modelling. Eur J Agron, 2019, 103: 13-23.

[31] Michel S, Loschenberger F, Hellinger J, et al. . Improving and maintaining winter hardiness and frost tolerance in bread wheat by genomic selection. Front Plant Sci, 2019, 101195

[32] Mickelbart MV, Hasegawa PM, Bailey-Serres J. Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat Rev Genet, 2015, 16: 237-251.

[33] Nei M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 1978, 89: 583-590.

[34] Pang YL, Wu YY, Liu CX, et al. . High-resolution genome-wide association study and genomic prediction for disease resistance and cold tolerance in wheat. Theor Appl Genet, 2021, 134: 2857-2873.

[35] Papagiannaki K, Lagouvardos K, Kotroni V, et al. . Agricultural losses related to frost events: use of the 850 hPa level temperature as an explanatory variable of the damage cost. Nat Hazard, 2014, 14: 2375-2386.

[36] Raper TB, Varco JJ. Canopy-scale wavelength and vegetative index sensitivities to cotton growth parameters and nitrogen status. Precision Agric, 2014, 16: 62-76.

[37] Rezaei EE, Webber H, Asseng S, et al. . Climate change impacts on crop yields. Nat Rev Earth Environ, 2023

[38] Saijo Y, Hata S, Kyozuka J, et al. . Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J, 2000, 23: 319-327.

[39] Saijo Y, Kinoshita N, Ishiyama K, et al. . A Ca(2+)-dependent protein kinase that endows rice plants with cold- and salt-stress tolerance functions in vascular bundles. Plant Cell Physiol, 2001, 42: 1228-1233.

[40] Sarić R, Nguyen VD, Burge T, et al. . Applications of hyperspectral imaging in plant phenotyping. Trends Plant Sci, 2022, 27: 301-315.

[41] Shi Y, Ding Y, Yang S. Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci, 2018, 23: 623-637.

[42] Soleimani B, Lehnert H, Babben S, et al. . Genome wide association study of frost tolerance in wheat. Sci Rep, 2022, 12: 5275

[43] Stutsel BM, Callow JN, Flower KC, et al. . Application of distributed temperature sensing using optical fibre to understand temperature dynamics in wheat (triticum aestivum) during frost. Eur J Agron, 2020, 115126038

[44] Sutka J, Snape JW. Location of a gene for frost resistance on chromosome 5A of wheat. Euphytica, 1989, 42: 41-44.

[45] Thompson CN, Guo WX, Sharma B, et al. . Using normalized difference red edge index to assess maturity in cotton. Crop Sci, 2019, 59: 2167-2177.

[46] Vágújfalvi A, Galiba G, Dubcovsky J, et al. . Two loci on wheat chromosome 5A regulate the differential cold-dependent expression of the cor14b gene in frost-tolerant and frost-sensitive genotypes. Mol Gen Genet MGG, 2000, 263: 194-200.

[47] Vagujfalvi A, Galiba G, Cattivelli L, et al. . The cold-regulated transcriptional activator Cbf3 is linked to the frost-tolerance locus Fr-A2 on wheat chromosome 5A. Mol Genet Genomics, 2003, 269: 60-67.

[48] Wang W, Guo W, Le L, et al. . Integration of high-throughput phenotyping, GWAS, and predictive models reveals the genetic architecture of plant height in maize. Mol Plant, 2023, 16: 354-373.

[49] Wu C, Niu Z, Tang Q, et al. . Estimating chlorophyll content from hyperspectral vegetation indices: Modeling and validation. Agric for Meteorol, 2008, 148: 1230-1241.

[50] Wu J, Yu R, Wang H, et al. . A large-scale genomic association analysis identifies the candidate causal genes conferring stripe rust resistance under multiple field environments. Plant Biotechnol J, 2020, 19: 177-191.

[51] Wu X, Feng H, Wu D, et al. . Using high-throughput multiple optical phenotyping to decipher the genetic architecture of maize drought tolerance. Genome Biology, 2021, 22185

[52] Wurschum T, Longin CF, Hahn V, et al. . Copy number variations of CBF genes at the Fr-A2locus are essential components of winter hardiness in wheat. Plant J, 2017, 89: 764-773.

[53] Xiao L, Liu L, Asseng S, et al. . Estimating spring frost and its impact on yield across winter wheat in China. Agric For Meteorol, 2018, 260–261: 154-164.

[54] Xiao J, Liu B, Yao YY, et al. . Wheat genomic study for genetic improvement of traits in China. Sci China Life Sci, 2022, 65: 1718-1775.

[55] Xue X, He T, Xu L, et al. . Quantifying the spatial pattern of urban heat islands and the associated cooling effect of blue–green landscapes using multisource remote sensing data. Sci Total Environ, 2022, 843156829

[56] Yan L, Fu D, Li C, et al. . The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA, 2006, 103: 19581-19586.

[57] Yano K, Yamamoto E, Aya K, et al. . Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice. Nat Genet, 2016, 48: 927-934.

[58] Yin Q, Zhang Y, Li W, et al. . Better inversion of wheat canopy SPAD values before heading stage using spectral and texture indices based on UAV multispectral imagery. Remote Sensing, 2023, 154935

[59] Yu S, Wu J, Wang M, et al. . Haplotype variations in QTL for salt tolerance in Chinese wheat accessions identified by marker-based and pedigree-based kinship analyses. Crop J, 2020, 8: 1011-1024.

[60] Yu R, Cao XF, Liu J, et al. . Using UAV-based temporal spectral indices to dissect changes in the stay-green trait in wheat. Plant Phenomics, 2024, 6: 0171

[61] Yue Y, Zhou Y, Wang JA, et al. . Assessing wheat frost risk with the support of GIS: An approach coupling a growing season meteorological index and a hybrid fuzzy neural network model. Sustainability, 2016, 8: 1308.

[62] Zhang H, Zhu J, Gong Z, et al. . Abiotic stress responses in plants. Nat Rev Genet, 2021, 23: 104-119.

[63] Zhang J, Islam MDS, Zhao Y, et al. . Non-escaping frost tolerant QTL linked genetic loci at reproductive stage in six wheat DH populations. Crop J, 2022, 10: 147-165.

[64] Zhang N, Huo W, et al. . Identification of winter-responsive proteins in bread wheat using proteomics analysis and virus-induced gene silencing (VIGS). Mol Cell Proteomics, 2016, 15(9): 2954-2969.

[65] Zhang N, Zhang L, Zhao L, et al. . iTRAQ and virus-induced gene silencing revealed three proteins involved in cold response in bread wheat. Sci Rep, 2017, 7: 7524

[66] Zhang N, Wang S, Zhao S, et al. . Global crotonylatome and GWAS revealed a TaSRT1-TaPGK model regulating wheat cold tolerance through mediating pyruvate. Sci Adv, 2023, 9eadg1012

[67] Zhao Y, Li J, Zhao R, et al. . Genome-wide association study reveals the genetic basis of cold tolerance in wheat. Mol Breed, 2020, 4036

[68] Zhou X, Stephens M (2012) Genome-wide efficient mixed-model analysis for association studies. Nat Genet 44:821-U136. https://doi.org/10.1038/ng.2310

[69] Zhu J, Pearce S, Burke A, et al. . Copy number and haplotype variation at the VRN-A1 and central FR-A2 loci are associated with frost tolerance in hexaploid wheat. Theor Appl Genet, 2014, 127: 1183-1197.

Funding

National Key R&D Program of China(No.2022YFE0116200)

Key Technologies Research and Development Program of Anhui Province(2022-NK-125)

Guangdong Provincial Introduction of Innovative Research and Development Team(grant no. Ylzy-xm-01)

RIGHTS & PERMISSIONS

The Author(s)