Field screening for heat-stress tolerance of floret fertility in wheat (Triticum aestivum and T. durum)
Livinus Emebiri
A * , Million F. Erena B , Kerry Taylor A , Shane Hildebrand A , Marco Maccaferri C and Nicholas C. Collins B
A
B
C
Abstract
As global temperatures increase, heat waves of >30°C for at least 3 days are projected to become more frequent during reproductive development of wheat, causing reductions in grain yield. Breeding for tolerance is difficult under field conditions owing to the unpredictable timing and intensity of natural heat events and the narrow developmental windows of sensitivity.
We report on a series of experiments designed to explore genetic variability for floret sterility induced by natural heat waves in the field by targeting a sensitive development stage.
Our method involved sowing late, and the use of auricle distance to identify main tillers exposed to heat events at a sensitive developmental stage (booting).
Substantial genetic variation was found for tolerance of grain set to natural heat waves, with a broad-sense heritability estimate of 0.94 for heat-exposed stems compared with 0.72 for non-stressed controls. An auricle distance of 1–3 cm was established as a phenotypic marker for tagging stems at the sensitive stage of development, and the optimal number of spikes to assess was determined as 10–15 per plot. A validation study with durum lines previously classified as tolerant/intolerant under glasshouse conditions showed agreement in ranking of genotypes at the extremes of tolerance.
We demonstrate that it is possible to screen wheat genotypes for stage-specific tolerance to natural heat waves in the field.
The protocol described could provide a low-cost method for evaluating heat tolerance in wheat, with relevance to commercial field production conditions. The approach allows tolerance to be assessed at a single stage of reproductive development, which should allow greater heritability in field assessments.
Keywords: abiotic tolerance, auricle distance, floret fertility, flowering stage, global climate change, heat stress, heat tolerance, Triticum spp., wheat.
References
Ababaei B, Chenu K (2020) Heat shocks increasingly impede grain filling but have little effect on grain setting across the Australian wheatbelt. Agricultural and Forest Meteorology 284, 107889.
| Crossref | Google Scholar |
Arias P, Bellouin N, Coppola E, Jones R, Krinner G, Marotzke J, Naik V, Palmer M, Plattner GK, Rogelj J, Rojas M (2021) ‘Climate change 2021: the physical science basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change; technical summary.’ (Cambridge University Press: Cambridge, UK; New York, NY, USA)
Asseng S, Ewert F, Martre P, Rötter RP, Lobell DB, Cammarano D, Kimball BA, Ottman MJ, Wall GW, White JW, et al. (2015) Rising temperatures reduce global wheat production. Nature Climate Change 5(2), 143-147.
| Crossref | Google Scholar |
Barber HM, Lukac M, Simmonds J, Semenov MA, Gooding MJ (2017) Temporally and genetically discrete periods of wheat sensitivity to high temperature. Frontiers in Plant Science 8, 51.
| Crossref | Google Scholar | PubMed |
Barton DA, Cantrill LC, Law AMK, Phillips CG, Sutton BG, Overall RL (2014) Chilling to zero degrees disrupts pollen formation but not meiotic microtubule arrays in Triticum aestivum L. Plant, Cell & Environment 37(12), 2781-2794.
| Crossref | Google Scholar | PubMed |
Bokshi AI, Tan DKY, Thistlethwaite RJ, Trethowan R, Kunz K (2021) Impact of elevated CO2 and heat stress on wheat pollen viability and grain production. Functional Plant Biology 48(5), 503-514.
| Crossref | Google Scholar | PubMed |
Browne RG, Li SF, Iacuone S, Dolferus R, Parish RW (2021) Differential responses of anthers of stress tolerant and sensitive wheat cultivars to high temperature stress. Planta 254(1), 4.
| Crossref | Google Scholar |
Brás TA, Seixas J, Carvalhais N, Jägermeyr J (2021) Severity of drought and heatwave crop losses tripled over the last five decades in Europe. Environmental Research Letters 16(6), 065012.
| Crossref | Google Scholar |
Calderini DF, Savin R, Abeledo LG, Reynolds MP, Slafer GA (2001) The importance of the period immediately preceding anthesis for grain weight determination in wheat. Euphytica 119(1), 199-204.
| Crossref | Google Scholar |
Coast O, Posch BC, Rognoni BG, Bramley H, Gaju O, Mackenzie J, Pickles C, Kelly AM, Lu M, Ruan Y-L, Trethowan R, Atkin OK (2022) Wheat photosystem II heat tolerance: evidence for genotype-by-environment interactions. The Plant Journal 111(5), 1368-1382.
| Crossref | Google Scholar | PubMed |
Cocks NA, March TJ, Biddulph TB, Smith AB, Cullis BR (2019) The provision of grower and breeder information on the frost susceptibility of wheat in Australia. The Journal of Agricultural Science 157(5), 382-398.
| Crossref | Google Scholar |
Collins B (2021) Frequency of compound hot–dry weather extremes has significantly increased in Australia since 1889. Journal of Agronomy and Crop Science 208, 941-955.
| Crossref | Google Scholar |
Collins NC, Hildebrand S, Taylor K, Taylor H, Plemin, D, Lohraseb I, Shirdelmoghanloo H, Erena M, Rahman M, Taylor J, Munoz-Santa S, Mather D, Heuer S, Sissons M, Emebiri L (2017) Understanding heat impacts on wheat to breed future tolerance. (Grains Research & Development Corporation: Canberra, Australia). Available at https://grdc.com.au/resources-and-publications/grdc-update-papers/tab-content/grdc-update-papers/2017/02/understanding-heat-impacts-on-wheat-to-breed-future-tolerance [Accessed 18 November 2023]
Craufurd PQ, Vadez V, Jagadish SVK, Prasad PVV, Zaman-Allah M (2013) Crop science experiments designed to inform crop modeling. Agricultural and Forest Meteorology 170, 8-18.
| Crossref | Google Scholar |
Cullis BR, Smith AB, Coombes NE (2006) On the design of early generation variety trials with correlated data. Journal of Agricultural, Biological, and Environmental Statistics 11(4), 381-393.
| Crossref | Google Scholar |
Dolferus R, Thavamanikumar S, Sangma H, Kleven S, Wallace X, Forrest K, Rebetzke G, Hayden M, Borg L, Smith A, Cullis B (2019) Determining the genetic architecture of reproductive stage drought tolerance in wheat using a correlated trait and correlated marker effect model. G3 Genes|Genomes|Genetics 9(2), 473-489.
| Crossref | Google Scholar | PubMed |
Draeger T, Moore G (2017) Short periods of high temperature during meiosis prevent normal meiotic progression and reduce grain number in hexaploid wheat (Triticum aestivum L.). Theoretical and Applied Genetics 130(9), 1785-1800.
| Crossref | Google Scholar | PubMed |
Erena MF, Lohraseb I, Munoz-Santa I, Taylor JD, Emebiri LC, Collins NC (2021) The WtmsDW locus on wheat chromosome 2B controls major natural variation for floret sterility responses to heat stress at booting stage. Frontiers in Plant Science 12, 635397.
| Crossref | Google Scholar | PubMed |
Farooq M, Bramley H, Palta JA, Siddique KHM (2011) Heat stress in wheat during reproductive and grain-filling phases. Critical Reviews in Plant Sciences 30, 491-507.
| Crossref | Google Scholar |
Feng F, Han Y, Wang S, Yin S, Peng Z, Zhou M, Gao W, Wen X, Qin X, Siddique KHM (2018) The effect of grain position on genetic improvement of grain number and thousand grain weight in winter wheat in North China. Frontiers in Plant Science 9, 129.
| Crossref | Google Scholar | PubMed |
Ferrante A, Savin R, Slafer GA (2013) Floret development and grain setting differences between modern durum wheats under contrasting nitrogen availability. Journal of Experimental Botany 64, 169-184.
| Crossref | Google Scholar | PubMed |
Fleury D, Jefferies S, Kuchel H, Langridge P (2010) Genetic and genomic tools to improve drought tolerance in wheat. Journal of Experimental Botany 61(12), 3211-3222.
| Crossref | Google Scholar | PubMed |
Guo Z, Schnurbusch T (2015) Variation of floret fertility in hexaploid wheat revealed by tiller removal. Journal of Experimental Botany 66(19), 5945-5958.
| Crossref | Google Scholar | PubMed |
Guo J, Zhang Y, Shi W, Zhang B, Zhang J, Xu Y, Cheng X, Cheng K, Zhang X, Hao C, Cheng S (2015) Association analysis of grain-setting rates in apical and basal spikelets in bread wheat (Triticum aestivum L.). Frontiers in Plant Science 6, 1029.
| Google Scholar | PubMed |
Hasegawa T, Ishimaru T, Kondo M, Kuwagata T, Yoshimoto M, Fukuoka M (2011) Spikelet sterility of rice observed in the record hot summer of 2007 and the factors associated with its variation. Journal of Agricultural Meteorology 67(4), 225-232.
| Crossref | Google Scholar |
Hays DB, Do JH, Mason RE, Morgan G, Finlayson SA (2007) Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar. Plant Science 172(6), 1113-1123.
| Crossref | Google Scholar |
Izanloo A, Condon AG, Langridge P, Tester M, Schnurbusch T (2008) Different mechanisms of adaptation to cyclic water stress in two South Australian bread wheat cultivars. Journal of Experimental Botany 59, 3327-3346.
| Crossref | Google Scholar | PubMed |
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 & Environment 33(6), 926-942 10.1111/j.1365-3040.2010.02130.x.
| Google Scholar |
Kim J, Slafer GA, Savin R (2021) Are portable polyethylene tents reliable for imposing heat treatments in field-grown wheat? Field Crops Research 271, 108206.
| Crossref | Google Scholar |
Kirby EJM (1974) Ear development in spring wheat. The Journal of Agricultural Science 82, 437-447.
| Crossref | Google Scholar |
Kozak M, Piepho H-P (2018) What’s normal anyway? Residual plots are more telling than significance tests when checking ANOVA assumptions. Journal of Agronomy and Crop Science 204(1), 86-98.
| Crossref | Google Scholar |
Leske B, Biddulph B, D’Antuono M, Onyemaobi IF, Colmer T (2019) Sample size is critical when exploring the grain set in wheat cultivars grown under frost-prone field conditions in Western Australia. In ‘Proceedings of the 2019 Agronomy Australia Conference, Wagga Wagga, Australia’. (The Australian Society of Agronomy). Available at http://agronomyaustraliaproceedingsorg/indexphp [Accessed 16 November 2021]
Li C, Peng C, Zhao Q, Xie P, Zuo W (2004) Characteristic analysis of the abnormal high temperature in 2003’s midsummer in Wuhan City. Journal of Central China Normal University (Natural Sciences) 38(3), 379-382.
| Google Scholar |
Liu H, Searle IR, Mather DE, Able AJ, Able JA (2015) Morphological, physiological and yield responses of durum wheat to pre-anthesis water-deficit stress are genotype-dependent. Crop & Pasture Science 66(10), 1024-1038.
| Crossref | Google Scholar |
Lobell DB, Hammer GL, Chenu K, Zheng B, McLean G, Chapman SC (2015) The shifting influence of drought and heat stress for crops in northeast Australia. Global Change Biology 21, 4115-4127.
| Crossref | Google Scholar | PubMed |
Maccaferri M, Sanguineti MC, Natoli V, Ortega JLA, Salem MB, Bort J, Chenenaoui C, De Ambrogio E, del Moral LG, De Montis A, El-Ahmed A, Maalouf F, Machlab H, Moragues M, Motawaj J, Nachit M, Nserallah N, Ouabbou H, Royo C, Tuberosa R (2006) A panel of elite accessions of durum wheat (Triticum durum Desf.) suitable for association mapping studies. Plant Genetic Resources 4(1), 79-85.
| Crossref | Google Scholar |
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. Journal of Experimental Botany 62(2), 409-438.
| Crossref | Google Scholar | PubMed |
Mason RE, Mondal S, Beecher FW, Pacheco A, Jampala B, Ibrahim AMH, Hays DB (2010) QTL associated with heat susceptibility index in wheat (Triticum aestivum L.) under short-term reproductive stage heat stress. Euphytica 174(3), 423-436.
| Crossref | Google Scholar |
Mirosavljević M, Mikić S, Špika AK, Župunski V, Zhou R, Abdelhakim L, Ottosen C-O (2021) The effect of heat stress on some main spike traits in 12 wheat cultivars at anthesis and mid-grain filling stage. Plant, Soil and Environment 67(2), 71-76.
| Crossref | Google Scholar |
Morgan JM (1980) Possible role of abscisic acid in reducing seed set in water-stressed wheat plants. Nature 285, 655-657.
| Crossref | Google Scholar |
Omidi M, Siahpoosh MR, Mamghani R, Modarresi M (2014) The influence of terminal heat stress on meiosis abnormalities in pollen mother cells of wheat. Cytologia 79(1), 49-58.
| Crossref | Google Scholar |
Onyemaobi I, Liu H, Siddique KHM, Yan G (2017) Both male and female malfunction contributes to yield reduction under water stress during meiosis in bread wheat. Frontiers in Plant Science 7, 2071.
| Crossref | Google Scholar |
Onyemaobi O, Sangma H, Garg G, Wallace X, Kleven S, Suwanchaikasem P, Roessner U, Dolferus R (2021) Reproductive stage drought tolerance in wheat: importance of stomatal conductance and plant growth regulators. Genes 12(11), 1742.
| Crossref | Google Scholar |
Passioura J (2006) Increasing crop productivity when water is scarce–from breeding to field management. Agricultural Water Management 80(1–3), 176-196.
| Crossref | Google Scholar |
Porter JR, Gawith M (1999) Temperatures and the growth and development of wheat: a review. European Journal of Agronomy 10(1), 23-36.
| Crossref | Google Scholar |
Prasad PVV, 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. Functional Plant Biology 41(12), 1261-1269.
| Crossref | Google Scholar | PubMed |
Qian CM, Xu A, Liang GH (1986) Effects of low temperatures and genotypes on pollen development in wheat. Crop Science 26(1), 43-46.
| Crossref | Google Scholar |
R Core Team (2021) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at https://wwwR-projectorg/
Reinheimer JL, Barr AR, Eglinton JK (2004) QTL mapping of chromosomal regions conferring reproductive frost tolerance in barley (Hordeum vulgare L.). Theoretical and Applied Genetics 109, 1267-1274.
| Crossref | Google Scholar | PubMed |
Richards RA (2006) Physiological traits used in the breeding of new cultivars for water-scarce environments. Agricultural Water Management 80, 197-211.
| Crossref | Google Scholar |
Sadras VO, Vadez V, Purushothaman R, Lake L, Marrou H (2015) Unscrambling confounded effects of sowing date trials to screen for crop adaptation to high temperature. Field Crops Research 177, 1-8.
| Crossref | Google Scholar |
Saini HS, Aspinall D (1982) Abnormal sporogenesis in wheat (Triticum aestivum L.) induced by short periods of high temperature. Annals of Botany 49(6), 835-846.
| Crossref | Google Scholar |
Sharma DL, Anderson WK (2004) Small grain screenings in wheat: interactions of cultivars with season, site, and management practices. Australian Journal of Agricultural Research 55(7), 797-809.
| Crossref | Google Scholar |
Shew AM, Tack JB, Nalley LL, Chaminuka P (2020) Yield reduction under climate warming varies among wheat cultivars in South Africa. Nature Communications 11(1), 4408.
| Crossref | Google Scholar |
Shirdelmoghanloo H, Taylor JD, Lohraseb I, Rabie H, Brien C, Timmins A, Martin P, Mather DE, Emebiri L, Collins NC (2016a) A QTL on the short arm of wheat (Triticum aestivum L.) chromosome 3B affects the stability of grain weight in plants exposed to a brief heat shock early in grain filling. BMC Plant Biology 16(1), 100.
| Crossref | Google Scholar |
Shirdelmoghanloo H, Cozzolino D, Lohraseb I, Collins NC (2016b) Truncation of grain filling in wheat (Triticum aestivum) triggered by brief heat stress during early grain filling: association with senescence responses and reductions in stem reserves. Functional Plant Biology 43(10), 919-930.
| Crossref | Google Scholar | PubMed |
Sissons M, Pleming D, Taylor JD, Emebiri L, Collins NC (2018) Effects of heat exposure from late sowing on the agronomic and technological quality of tetraploid wheat. Cereal Chemistry 95(2), 274-287.
| Crossref | Google Scholar |
Slafer GA, Elia M, Savin R, García GA, Terrile II, Ferrante A, Miralles DJ, González FG (2015) Fruiting efficiency: an alternative trait to further rise wheat yield. Food and Energy Security 4(2), 92-109.
| Crossref | Google Scholar |
Stone PJ, Nicolas ME (1995) Effect of timing of heat stress during grain filling on two wheat varieties differing in heat tolerance. I. Grain growth. Functional Plant Biology 22(6), 927-934.
| Crossref | Google Scholar |
Tack J, Barkley A, Nalley LL (2015) Effect of warming temperatures on US wheat yields. Proceedings of the National Academy of Sciences USA 112(22), 6931-6936.
| Crossref | Google Scholar |
Tack J, Barkley A, Hendricks N (2017) Irrigation offsets wheat yield reductions from warming temperatures. Environmental Research Letters 12(11), 114027.
| Crossref | Google Scholar |
Tashiro T, Wardlaw IF (1990) The response to high temperature shock and humidity changes prior to and during the early stages of grain development in wheat. Functional Plant Biology 17, 551-561.
| Crossref | Google Scholar |
Templ B, Calanca P (2020) Critical increase in the occurrence of heat stress during reproductive growth in Russian wheat beyond 1.5 C global warming. Weather and Climate Extremes 30, 100281.
| Crossref | Google Scholar |
Thistlethwaite RJ, Tan DKY, Bokshi AI, Ullah S, Trethowan RM (2020) A phenotyping strategy for evaluating the high-temperature tolerance of wheat. Field Crops Research 255, 107905.
| Crossref | Google Scholar |
Tottman DR (1987) The decimal code for the growth stages of cereals, with illustrations. Annals of Applied Biology 110, 441-454.
| Crossref | Google Scholar |
Ugarte C, Calderini DF, Slafer GA (2007) Grain weight and grain number responsiveness to pre-anthesis temperature in wheat, barley and triticale. Field Crops Research 100(2–3), 240-248.
| Crossref | Google Scholar |
Ullah S, Bramley H, Mahmood T, Trethowan R (2020) A strategy of ideotype development for heat-tolerant wheat. Journal of Agronomy and Crop Science 206(2), 229-241.
| Crossref | Google Scholar |
Wardlaw IF (1994) The effect of high temperature on kernel development in wheat: variability related to pre-heading and post-anthesis conditions. Functional Plant Biology 21(6), 731-739.
| Crossref | Google Scholar |
Wardlaw IF, Wrigley CW (1994) Heat tolerance in temperate cereals: an overview. Australian Journal of Plant Physiology 21, 695-703.
| Google Scholar |
Wardlaw IF, Dawson IA, Munibi P, Fewster R (1989) The tolerance of wheat to high temperatures during reproductive growth. I. Survey procedures and general response patterns. Australian Journal of Agricultural Research 40(1), 1-13.
| Crossref | Google Scholar |
Wollenweber B, Porter JR, Schellberg J (2003) Lack of interaction between extreme high-temperature events at vegetative and reproductive growth stages in wheat. Journal of Agronomy and Crop Science 189(3), 142-150.
| Crossref | Google Scholar |
Xu J, Lowe C, Hernandez-Leon SG, Dreisigacker S, Reynolds MP, Valenzuela-Soto EM, Paul MJ, Heuer S (2022) The effects of brief heat during early booting on reproductive, developmental, and chlorophyll physiological performance in common wheat (Triticum aestivum L.). Frontiers in Plant Science 13, 886541.
| Crossref | Google Scholar | PubMed |
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Research 14(6), 415-421.
| Crossref | Google Scholar |
Zhang J, Dell B, Conocono E, Waters I, Setter T, Appels R (2009) Water deficits in wheat: fructan exohydrolase (1-FEH) mRNA expression and relationship to soluble carbohydrate concentrations in two varieties. New Phytologist 181(4), 843-850.
| Crossref | Google Scholar | PubMed |
Zhang J, Xu Y, Chen W, Dell B, Vergauwen R, Biddulph B, Khan N, Luo H, Appels R, Van den Ende W (2015) A wheat 1-FEH w3 variant underlies enzyme activity for stem WSC remobilization to grain under drought. New Phytologist 205(1), 293-305.
| Crossref | Google Scholar |
Zhao C, Liu B, Piao S, Wang X, Lobell DB, Huang Y, Huang M, Yao Y, Bassu S, Ciais P, Durand J-L, et al. (2017) Temperature increase reduces global yields of major crops in four independent estimates. Proceedings of the National Academy of Sciences USA 114(35), 9326-9331.
| Google Scholar |
