Deciphering genetic variation of terminal heat stress-responsive traits in Nepalese wheat germplasm using phenotyping and functional marker analysis

##plugins.themes.bootstrap3.article.main##

NABARAJ KHANAL
SAROJ PANTHI
MADHAV PRASAD PANDEY
HIMAL LUITEL
RITU RANI POUDEL
NABIN BHUSAL
https://orcid.org/0000-0003-2330-0391

Abstract

Abstract. Khanal N, Panthi S, Pandey MP, Luitel H, Poudel RR, Bhusal N. 2024. Deciphering genetic variation of terminal heat stress-responsive traits in Nepalese wheat germplasm using phenotyping and functional marker analysis. Asian J Agric 8: 134-141. Development of heat-tolerant wheat cultivars is becoming more essential for the food security due to the increasing impact of global warming. In the present study, Nepalese bread wheat accessions, along with the check varieties were evaluated under late-sown heat stress conditions, followed by genotyping of selected accessions using trait-based functional markers. The findings showed a reduction in Thousand-Grain Weight (TGW), Grain Weight per Spike (GWS), and Grain Filling Duration (GFD), due to the late-sown heat-stressed environment. The reduction for GFD and GWS among the wheat accessions ranged from 22.2 to 62.3% over the heat-tolerant check genotypes (NL-971 and Aditya), respectively. The correlation and principal component analysis showed that TGW, GWS, and GFD were positively associated with each other. The analysis of functional markers CWI21 and CWI22 (linked to TaCwi-A1 and TaCwi-A2 genes) and GS7D (linked to TaGS-D1a or TaGS-D1b genes) showed an association with the TGW. The accessions NGRC-02584 and NGRC-02602 possessed the positive alleles of markers CWI22 and GS7D for a higher TGW, indicating that these accessions have the potential to withstand terminal heat stress and could be included in breeding programs after validation.

2017-01-01

##plugins.themes.bootstrap3.article.details##

References
Abdelrahman M, Burritt DJ, Gupta A, Tsujimoto H, Tran LS. 2020. Heat stress effects on source-sink relationships and metabolome dynamics in wheat. J Exp Bot 71 (2): 543-554. DOI: 10.1093/jxb/erz296.
Ali MB, Ibrahim AM, Hays DB, Ristic Z, Fu J. 2010. Wild tetraploid wheat (Triticum turgidum L.) response to heat stress. J Crop Improv 24 (3): 228-243. DOI: 10.1080/15427528.2010.481523.
Anderson JA, Churchill GA, Autrique JE, Tanksley SD, Sorrells ME. 1993. Optimizing parental selection for genetic linkage maps. Genome 36(1):181-186. DOI: 10.1139/g93-024.
Aravind J, Mukesh Sankar S, Wankhede DP, Kaur V. 2021. Augmented RCBD: Analysis of Augmented Randomised Complete Block Designs. R package version 0.1.7. https://aravind-j.github.io/augmentedRCBD/https://cran.r-project.org/package=augmentedRCBD.
Aryal L, Shrestha SM, Khatri-Chhetri GB, Bhandari D. 2015. Chlorophyll content measurement of drought tolerant wheat genotypes sown at normal and late conditions as an indicator of spot blotch resistance. J Inst Agric Anim Sci 33: 65-72. DOI: 10.3126/jiaas.v33i0.20687.
Aziz A, Mahmood T, Mahmood Z, Shazadi K, Mujeeb?Kazi A, Rasheed A. 2018. Genotypic variation and genotype× environment interaction for yield?related traits in synthetic hexaploid wheats under a range of optimal and heat?stressed environments. Crop Sci 58 (1): 295-303. DOI: 10.2135/cropsci2017.01.0035.
Balla K, Karsai I, Bónis P, Kiss T, Berki Z, Horvath A, Mayer M, Bencze S, Veisz O. 2019. Heat stress responses in a large set of winter wheat cultivars (Triticum aestivum L.) depend on the timing and duration of stress. PLoS One 14 (9): e0222639. DOI: 10.1371/journal.pone.0222639.
Bednarek J, Boulaflous A, Girousse C, Ravel C, Tassy C, Barret P, Bouzidi MF, Mouzeyar S. 2012. Down-regulation of the TaGW2 gene by RNA interference results in decreased grain size and weight in wheat. J Exp Bot 63 (16): 5945-5955. DOI: 10.1093/jxb/ers249.
Bergkamp B, Impa SM, Asebedo AR, Fritz AK, Jagadish SK. 2018. Prominent winter wheat varieties response to post-flowering heat stress under controlled chambers and field-based heat tents. Field Crops Res 222: 143-152. DOI: 10.1016/j.fcr.2018.03.009.
Bhusal N, Sarial AK, Sharma P, Sareen S. 2017. Mapping QTLs for grain yield components in wheat under heat stress. PLoS One 12 (12): e0189594. DOI: 10.1371/journal.pone.0189594.
Brunner S, Hurni S, Streckeisen P, Mayr G, Albrecht M, Yahiaoui N, Keller B. 2010. Intragenic allele pyramiding combines different specificities of wheat Pm3 resistance alleles. Plant J 64 (3): 433-445. DOI: 10.1111/j.1365-313X.2010.04342.x.
Chang JZ, Hao CY, Chang XP, Zhang XY, Jing RL. 2014. HapIII of TaSAP1-A1, a positively selected haplotype in wheat breeding. J Integr Agric 13 (7): 1462-1468. DOI: 10.1016/S2095-3119(14)60808-X.
Choulet F, Caccamo M, Wright J, Alaux M, Šimková H, Šafá? J, Leroy P, Doležel J, Rogers J, Eversole K, Feuillet C. 2014. The wheat black jack: advances towards sequencing the 21 chromosomes of bread wheat. In: Tuberosa R, Graner A, Frison E (eds). Genomics of Plant Genetic Resources: Volume 1. Managing, sequencing and mining genetic resources. Springer, Dordrecht. DOI: 10.1007/978-94-007-7572-5_17.
Deutsch CA, Tewksbury JJ, Tigchelaar M, Battisti DS, Merrill SC, Huey RB, Naylor RL. 2018. Increase in crop losses to insect pests in a warming climate. Science 361: 916-919. DOI: 10.1126/science.aat3466.
Dias AS, Bagulho AS, Lidon FC. 2008. Ultrastructure and biochemical traits of bread and durum wheat grains under heat stress. Braz J Plant Physiol 20: 323-333. DOI: 10.1590/S1677-04202008000400008.
Distelfeld A, Uauy C, Fahima T, Dubcovsky J. 2006. Physical map of the wheat high?grain protein content gene Gpc?B1 and development of a high?throughput molecular marker. New Phytol 169 (4): 753-763. DOI: 10.1111/j.1469-8137.2005.01627.x.
Fan Y, Ma C, Huang Z, Abid M, Jiang S, Dai T, Zhang W, Ma S, Jiang D, Han X. 2018. Heat priming during early reproductive stages enhances thermo-tolerance to post-anthesis heat stress via improving photosynthesis and plant productivity in winter wheat (Triticum aestivum L.). Front Plant Sci 9: 805. DOI: 10.3389/fpls.2018.00805.
Farooq M, Bramley H, Palta JA, Siddique KH. 2011. Heat stress in wheat during reproductive and grain-filling phases. Crit Rev Plant Sci 30 (6): 491-507. DOI: 10.1080/07352689.2011.615687.
IPCC Secretariat. 2021. Scientific Review of the Impact of Climate Change on Plant Pests—A Global Challenge to Prevent and Mitigate Plant Pest Risks in Agriculture, Forestry and Ecosystems. FAO on Behalf of the IPCC Secretariat, Rome. DOI: 10.4060/cb4769en.
IPCC. 2022. Climate Change 2022: Mitigation of Climate Change. Contribution of Working Group iii to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change; Cambridge University Press, Cambridge, UK.
Jiang Q, Hou J, Hao C, Wang L, Ge H, Dong Y, Zhang X. 2011. The wheat (T. aestivum) sucrose synthase 2 gene (TaSus2) active in endosperm development is associated with yield traits. Funct Integr Genom 11: 49-61. DOI: 10.1007/s10142-010-0188-x.
Joshi AK, Mishra B, Chatrath R, Ortiz Ferrara G, Singh RP. 2007. Wheat improvement in India: present status, emerging challenges and future prospects. Euphytica 157: 431-446. DOI: 10.1007/s10681-007-9385-7.
Kajla M, Yadav VK, Chhokar RS, Sharma RK. 2015. Management practices to mitigate the impact of high temperature on wheat. J Wheat Res 7 (1): 11-22. DOI: 10.31018/jans.v7i2.733.
Kumar S, Kumari J, Bhusal N, Pradhan AK, Budhlakoti N, Mishra DC, Chauhan D, Kumar S, Singh AK, Reynolds M, Singh GP. 2020. Genome-wide association study reveals genomic regions associated with ten agronomical traits in wheat under late-sown conditions. Front Plant Sci 11: 549743. DOI: 10.3389/fpls.2020.549743.
Liu B, Asseng S, Müller C et al. 2016. Similar estimates of temperature impacts on global wheat yield by three independent methods. Nat Clim Chang 6: 1130-1136. DOI: 10.1038/nclimate3115.
Ma D, Yan J, He Z, Wu L, Xia X. 2012. Characterization of a cell wall invertase gene TaCwi-A1 on common wheat chromosome 2A and development of functional markers. Mol Breed 29: 43-52. DOI: 10.1007/s11032-010-9524-z.
Mahrookashani A, Siebert S, Hüging H, Ewert F. 2017. Independent and combined effects of high temperature and drought stress around anthesis on wheat. J Agron Crop Sci 203 (6): 453-463. DOI: 10.1111/jac.12218.
Martin JM, Meyer FD, Smidansky ED, Wanjugi H, Blechl AE, Giroux MJ. 2006. Complementation of the pina (null) allele with the wild type Pina sequence restores a soft phenotype in transgenic wheat. Theor Appl Genet 113: 1563-1570. DOI: 10.1007/s00122-006-0404-1.
Mishra SC, Singh S, Patil R, Bhusal N, Malik A, Sareen S, Shukla RS, Mishra PC, Chatrath R, Gupta RK, Tomar SS. 2014. Breeding for heat tolerance in wheat. Genetics 2 (1): 15-29.
Mondal S, Singh RP, Crossa J, Huerta-Espino J, Sharma I, Chatrath R, Singh GP et al. 2013. Earliness in wheat: a key to adaptation under terminal and continual high temperature stress in South Asia. Field Crops Res 151: 19-26. DOI: 10.1016/j.fcr.2013.06.015.
Mottaleb KA, Kruseman G, Frija A, Sonder K, Lopez-Ridaura S. 2023. Projecting wheat demand in China and India for 2030 and 2050: Implications for food security. Front Nutr 9: 1077443. DOI: 10.3389/fnut.2022.1077443.
Mukherjee D. 2012. Effect of different sowing dates on growth and yield of wheat (Triticum aestivum) cultivars under mid hill situation of West Bengal. Indian J Agronom 57 (2): 152-156. DOI: 10.59797/ija.v57i2.4627.
Munsif F, Arif M, Ali K, Khan MJ, Munir S, Rasul F. 2016. Evaluation of various morpho-physiological and growth traits of dual-purpose wheat under early sowing dates. Pak J Bot 48: 81-88.
Nadolska-Orczyk A, Rajchel IK, Orczyk W, Gasparis S. 2017. Major genes determining yield-related traits in wheat and barley. Theor Appl Genet 130: 1081-1098. DOI: 10.1007/s00122-017-2880-x.
Perrier X, Jacquemoud-Collet JP. 2006. DARwin Software. http://darwin.cirad.fr/darwin.
Prasad PV, Djanaguiraman M. 2014. Response of floret fertility and individual grain weight of wheat to high temperature stress: Sensitive stages and thresholds for temperature and duration. Funct Plant Biol 41 (12): 1261-1269. DOI: 10.1071/FP14061.
Puri RR, Gautam NR, Joshi AK. 2015. Exploring stress tolerance indices to identify terminal heat tolerance in spring wheat in Nepal. J Wheat Res 7 (1): 13-17.
Rasheed A, Jin H, Xiao Y, Zhang Y, Hao Y, Zhang Y, Hickey LT, Morgounov AI, Xia X, He Z. 2019. Allelic effects and variations for key bread-making quality genes in bread wheat using high-throughput molecular markers. J Cereal Sci 85: 305-309. DOI: 10.1016/j.jcs.2018.12.004.
Rasheed A, Wen W, Gao F, Zhai S, Jin H, Liu J, Guo Q, Zhang Y, Dreisigacker S, Xia X, He Z. 2016. Development and validation of KASP assays for genes underpinning key economic traits in bread wheat. Theor Appl Genet 129: 1843-1860. DOI: 10.1007/s00122-016-2743-x.
Ray DK, Mueller ND, West PC, Foley JA. 2013. Yield trends are insufficient to double global crop production by 2050. PloS one 8 (6): e66428. DOI: 10.1371/journal.pone.0066428.
Robles-Zazueta CA, Crespo-Herrera LA, Piñera-Chavez FJ, Rivera-Amado C, Aradottir GI. 2024. Climate change impacts on crop breeding: Targeting interacting biotic and abiotic stresses for wheat improvement. Plant Genom 17: e20365. DOI: 10.1002/tpg2.20365.
RStudio Team, RStudio. 2015. Integrated Development Environment for R, Boston, MA. http://www.rstudio.com/
Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard R. 1984. Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci 81 (24): 8014-8018. DOI: 10.1073/pnas.81.24.8014.
Sareen S, Tyagi BS, Sarial AK, Tiwari V, Sharma I. 2014. Trait analysis, diversity, and genotype x environment interaction in some wheat landraces evaluated under drought and heat stress conditions. Chilean J Agric Res 74 (2): 135-142. DOI: 10.4067/S0718-58392014000200002.
Schittenhelm S, Langkamp?Wedde T, Kraft M, Kottmann L, Matschiner K. 2020. Effect of two?week heat stress during grain filling on stem reserves, senescence, and grain yield of European winter wheat cultivars. J Agron Crop Sci 206 (6): 722-733. DOI: 10.1111/jac.12410.
Sehgal D, Mondal S, Guzman C, Garcia Barrios G, Franco C, Singh R, Dreisigacker S. 2019. Validation of candidate gene-based markers and identification of novel loci for thousand-grain weight in spring bread wheat. Front Plant Sci 10: 1189. DOI: 10.3389/fpls.2019.01189.
Semenov MA, Stratonovitch P, Alghabari F, Gooding MJ. 2014. Adapting wheat in Europe for climate change. J Cereal Sci 59 (3): 245-256. DOI: 10.1016/j.jcs.2014.01.006.
Su Z, Hao C, Wang L, Dong Y, Zhang X. 2011. Identification and development of a functional marker of TaGW2 associated with grain weight in bread wheat (Triticum aestivum L.). Theor Appl Genet 122: 211-223. DOI: 10.1007/s00122-010-1437-z.
Talukder AS, McDonald GK, Gill GS. 2014. Effect of short-term heat stress prior to flowering and early grain set on the grain yield of wheat. Field Crops Res 160: 54-63. DOI: 10.1016/j.fcr.2014.01.013.
Thapa RS, Sharma PK, Pratap D, Singh T, Kumar A. 2019. Assessment of genetic variability, heritability and genetic advance in wheat (Triticum aestivum L.) genotypes under normal and heat stress environment. Indian J Agric Res 53 (1): 51-56. DOI: 10.18805/IJARe.A-5095.
Tian Y, Liu P, Cui F, Xu H, Han X, Nie Y, Kong D, Sang W, Li W. 2023. Genome-wide association study for yield and yield-related traits in Chinese spring wheat. Agronomy 13 (11): 2784. DOI: 10.3390/agronomy13112784.
Wang X, Guan P, Xin M, Wang Y, Chen X, Zhao A, Liu M, Li H, Zhang M, Lu L, Zhang J, Ni Z, Yao Y, Hu Z, Peng H, Sun Q. 2021. Genome-wide association study identifies QTL for thousand grain weight in winter wheat under normal-and late-sown stressed environments. Theor Appl Genet 134: 143-157. DOI: 10.1007/s00122-020-03687-w.
Wei B, Jing R, Wang C, Chen J, Mao X, Chang X, Jia J. 2009. Dreb1 genes in wheat (Triticum aestivum L.): Development of functional markers and gene m apping based on SNPs. Mol Breed 23: 13-22. DOI: 10.1007/s11032-008-9209-z.
Yan H, Deng D, Zhou P, Peng Y, Dong X, Li S, Zhang Y, Man Q, Lv Z, Chen T, Ren C. 2023. Dissecting the genetic basis of grain weight and size in common oat by genome-wide association study. J Cereal Sci 2023: 103811. DOI: 10.1016/j.jcs.2023.103811.
Yang Z, Bai Z, Li X, Wang P, Wu Q, Yang L et al. 2012. SNP identification and allelic-specific PCR markers development for TaGW2, a gene linked to wheat kernel weight. Theor Appl Genet 125: 1057-1068. DOI: 10.1007/s00122-012-1895-6.
Zhang Y, Liu J, Xia X, He Z. 2014. TaGS-D1, an ortholog of rice OsGS3, is associated with grain weight and grain length in common wheat. Mol Breed 34: 1097-1107. DOI: 10.1007/s11032-014-0102-7.
Zhao C, Liu B, Piao S et al. 2017. Temperature increase reduces global yields of major crops in four independent estimates. Proc Natl Acad Sci 114: 9326-9331. DOI: 10.1073/pnas.1701762114.