Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE (Open Access)

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

Hamid Shirdelmoghanloo A , Daniel Cozzolino B C , Iman Lohraseb A and Nicholas C. Collins A D
+ Author Affiliations
- Author Affiliations

A The Australian Centre for Plant Functional Genomics, School of Agriculture Food and Wine, The University of Adelaide, PMB1 Glen Osmond, SA 5064, Australia.

B School of Agriculture Food and Wine, the University of Adelaide, PMB1 Glen Osmond, SA 5064, Australia.

C Present address: School of Medical and Applied Sciences, Central Queensland University, Rockhampton North Campus, Bruce Highway, Qld 4701, Australia.

D Corresponding author. Email: nick.collins@acpfg.com.au

Functional Plant Biology 43(10) 919-930 https://doi.org/10.1071/FP15384
Submitted: 22 December 2015  Accepted: 5 May 2016   Published: 1 August 2016

Journal Compilation © CSIRO Publishing 2016 Open Access CC BY-NC-ND

Abstract

Short heat waves during grain filling can reduce grain size and consequently yield in wheat (Triticum aestivum L.). Grain weight responses to heat represent the net outcome of reduced photosynthesis, increased mobilisation of stem reserves (water-soluble carbohydrates, WSC) and accelerated senescence in the grain. To compare their relative roles in grain weight responses under heat, these characteristics were monitored in nine wheat genotypes subjected to a brief heat stress at early grain filling (37°C maximum for 3 days at 10 days after anthesis). Compared with the five tolerant varieties, the four susceptible varieties showed greater heat-triggered reductions in final grain weight, grain filling duration, flag leaf chla and chlb content, stem WSC and PSII functionality (Fv/Fm). Despite the potential for reductions in sugar supply to the developing grains, there was little effect of heat on grain filling rate, suggesting that grain size effects of heat may have instead been driven by premature senescence in the grain. Extreme senescence responses potentially masked stem WSC contributions to grain weight stability. Based on these findings, limiting heat-triggered senescence in the grain may provide an appropriate focus for improving heat tolerance in wheat.

Additional keywords: grain weight, photosynthesis, stay-green, temperature, water-soluble carbohydrate.


References

Abbad H, El Jaafari S, Bort Pie J, Araus Ortega JL (2004) Comparison of flag leaf and ear photosynthesis with biomass and grain yield of durum wheat under various water conditions and genotypes. Agronomie 24, 19–28.
Comparison of flag leaf and ear photosynthesis with biomass and grain yield of durum wheat under various water conditions and genotypes.Crossref | GoogleScholarGoogle Scholar |

Al‐Khatib K, Paulsen GM (1984) Mode of high temperature injury to wheat during grain development. Physiologia Plantarum 61, 363–368.
Mode of high temperature injury to wheat during grain development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlt1OnsLo%3D&md5=3dc1498f21f29ec53f59dfd9150628eaCAS |

Araus J, Brown H, Febrero A, Bort J, Serret M (1993) Ear photosynthesis, carbon isotope discrimination and the contribution of respiratory CO2 to differences in grain mass in durum wheat. Plant, Cell & Environment 16, 383–392.
Ear photosynthesis, carbon isotope discrimination and the contribution of respiratory CO2 to differences in grain mass in durum wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlslOlt7k%3D&md5=b895be9ae35ecd054ade6ffb50ca97bcCAS |

Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1–15.
Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaH1MXhtFaqtg%3D%3D&md5=f047f798fba7c2e7b043de4bb1179c39CAS | 16654194PubMed |

Asseng S, Foster IAN, Turner NC (2011) The impact of temperature variability on wheat yields. Global Change Biology 17, 997–1012.
The impact of temperature variability on wheat yields.Crossref | GoogleScholarGoogle Scholar |

Bidinger F, Musgrave R, Fischer R (1977) Contribution of stored pre-anthesis assimilate to grain yield in wheat and barley. Nature 270, 431–433.
Contribution of stored pre-anthesis assimilate to grain yield in wheat and barley.Crossref | GoogleScholarGoogle Scholar |

Blum A, Sinmena B, Mayer J, Golan G, Shpiler L (1994) Stem reserve mobilisation supports wheat-grain filling under heat stress. Australian Journal of Plant Physiology 21, 771–781.
Stem reserve mobilisation supports wheat-grain filling under heat stress.Crossref | GoogleScholarGoogle Scholar |

Deery D, Jimenez-Berni J, Jones H, Sirault X, Furbank R (2014) Proximal remote sensing buggies and potential applications for field-based phenotyping. Agronomy 4, 349–379.
Proximal remote sensing buggies and potential applications for field-based phenotyping.Crossref | GoogleScholarGoogle Scholar |

Dreccer MF, Barnes LR, Meder R (2014) Quantitative dynamics of stem water soluble carbohydrates in wheat can be monitored in the field using hyperspectral reflectance. Field Crops Research 159, 70–80.
Quantitative dynamics of stem water soluble carbohydrates in wheat can be monitored in the field using hyperspectral reflectance.Crossref | GoogleScholarGoogle Scholar |

Georgieva K (1999) Some mechanisms of damage and acclimation of the photosynthetic apparatus due to high temperature. Bulgarian Journal of Plant Physiology 25, 89–99.

Haque MS, Kjaer KH, Rosenqvist E, Sharma DK, Ottosen CO (2014) Heat stress and recovery of photosystem II efficiency in wheat (Triticum aestivum L.) cultivars acclimated to different growth temperatures. Environmental and Experimental Botany 99, 1–8.
Heat stress and recovery of photosystem II efficiency in wheat (Triticum aestivum L.) cultivars acclimated to different growth temperatures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXislKqu74%3D&md5=88ee56cf46e9fb95eb93ce09d2e24797CAS |

Harding SA, Guikema JA, Paulsen GM (1990) Photosynthetic decline from high temperature stress during maturation of wheat I. Interaction with senescence processes. Plant Physiology 92, 648–653.
Photosynthetic decline from high temperature stress during maturation of wheat I. Interaction with senescence processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhslGrtro%3D&md5=22d9d9dca4d7725d6f8a3209163117e6CAS | 16667329PubMed |

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, 1113–1123.
Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFGitLw%3D&md5=163e058a5db7764a4552ca2d4e5ba41dCAS |

Hiscox JT, Israelstam G (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Canadian Journal of Botany 57, 1332–1334.
A method for the extraction of chlorophyll from leaf tissue without maceration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXltlKlsbg%3D&md5=e3be76c8c48580543dfbbbb4e51c106eCAS |

Hurkman WJ, McCue KF, Altenbach SB, Korn A, Tanaka CK, Kothari KM, Johnson EL, Bechtel DB, Wilson JD, Anderson OD (2003) Effect of temperature on expression of genes encoding enzymes for starch biosynthesis in developing wheat endosperm. Plant Science 164, 873–881.
Effect of temperature on expression of genes encoding enzymes for starch biosynthesis in developing wheat endosperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivFeqsbc%3D&md5=51b3a26328831ae9ab382b85ac184de5CAS |

Jenner C (1994) Starch synthesis in the kernel of wheat under high temperature conditions. Functional Plant Biology 21, 791–806.

Kumari M, Singh V, Tripathi R, Joshi A (2007) Variation for staygreen trait and its association with canopy temperature depression and yield traits under terminal heat stress in wheat. In ‘Wheat production in stressed environments.’ (Eds HT Buck, JE Nisi, N Salomón) pp. 357–363. (Springer: Dordrecht.)

Lopes MS, Reynolds MP (2012) Stay-green in spring wheat can be determined by spectral reflectance measurements (normalized difference vegetation index) independently from phenology. Journal of Experimental Botany 63, 3789–3798.
Stay-green in spring wheat can be determined by spectral reflectance measurements (normalized difference vegetation index) independently from phenology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVSht7jI&md5=ea34738739d3c02b42ce214fcd56cc43CAS | 22412185PubMed |

Loss S, Kirby E, Siddique K, Perry M (1989) Grain growth and development of old and modern Australian wheats. Field Crops Research 21, 131–146.
Grain growth and development of old and modern Australian wheats.Crossref | GoogleScholarGoogle Scholar |

Maphosa L, Collins N, Taylor J, Mather D (2014) Post-anthesis heat and a Gpc-B1 introgression have similar but non-additive effects in bread wheat. Functional Plant Biology 41, 1002–1008.
Post-anthesis heat and a Gpc-B1 introgression have similar but non-additive effects in bread wheat.Crossref | GoogleScholarGoogle Scholar |

McMaster GS (1997) Phenology, development, and growth of wheat (Triticum aestivum L.) shoot apex: a review. Advances in Agronomy 59, 63–118.
Phenology, development, and growth of wheat (Triticum aestivum L.) shoot apex: a review.Crossref | GoogleScholarGoogle Scholar |

R Development Core Team (2012) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at: http://www.R-project.org [Verified 16 May 2016]

Richardson AD, Duigan SP, Berlyn GP (2002) An evaluation of noninvasive methods to estimate foliar chlorophyll content. New Phytologist 153, 185–194.
An evaluation of noninvasive methods to estimate foliar chlorophyll content.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xns1yrsQ%3D%3D&md5=f9b5e6e4527cf84e0719337ede18613cCAS |

Ristic Z, Bukovnik U, Prasad PV (2007) Correlation between heat stability of thylakoid membranes and loss of chlorophyll in winter wheat under heat stress. Crop Science 47, 2067–2073.
Correlation between heat stability of thylakoid membranes and loss of chlorophyll in winter wheat under heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlSltbbN&md5=05c8e36d2104c8eaa3e381935f7b7a85CAS |

Ristic Z, Bukovnik U, Prasad P, West M (2008) A model for prediction of heat stability of photosynthetic membranes. Crop Science 48, 1513–1522.
A model for prediction of heat stability of photosynthetic membranes.Crossref | GoogleScholarGoogle Scholar |

Saini H, Aspinall D (1982) Abnormal sporogenesis in wheat (Triticum aestivum L.) induced by short periods of high temperature. Annals of Botany 49, 835–846.

Shirdelmoghanloo H, Taylor JD, Lohraseb I, Rabie H, Brien C, Timmins A, Martin P, Mather DE, Emebiri L, Collins NC (2016) 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, 100
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.Crossref | GoogleScholarGoogle Scholar | 27101979PubMed |

Sofield I, Evans L, Cook M, Wardlaw IF (1977) Factors influencing the rate and duration of grain filling in wheat. Functional Plant Biology 4, 785–797.

Stone P, Nicolas M (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, 927–934.

Talukder A, McDonald GK, Gill GS (2013) Effect of short-term heat stress prior to flowering and at early grain set on the utilization of water-soluble carbohydrate by wheat genotypes. Field Crops Research 147, 1–11.
Effect of short-term heat stress prior to flowering and at early grain set on the utilization of water-soluble carbohydrate by wheat genotypes.Crossref | GoogleScholarGoogle Scholar |

Talukder A, 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 Research 160, 54–63.
Effect of short-term heat stress prior to flowering and early grain set on the grain yield of wheat.Crossref | GoogleScholarGoogle Scholar |

Tashiro T, Wardlaw I (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.

Telfer P, Edwards J, Kuchel H, Reinheimer J, Bennett D (2013) ‘Heat stress tolerance of wheat.’ (Grains Research and Development Corporation: Barton, ACT) Available at: http://www.grdc.com.au/Research-and-Development/GRDC-Update-Papers/2013/02/Heat-stress-tolerance-of-wheat [Verified 16 May 2016]

van Herwaarden A, Farquhar G, Angus J, Richards R, Howe G (1998) ‘Haying-off’, the negative grain yield response of dryland wheat to nitrogen fertiliser: I. Biomass, grain yield, and water use. Australian Journal of Agricultural Research 49, 1067–1081.
‘Haying-off’, the negative grain yield response of dryland wheat to nitrogen fertiliser: I. Biomass, grain yield, and water use.Crossref | GoogleScholarGoogle Scholar |

Vignjevic M, Wang X, Olesen J, Wollenweber B (2015) Traits in spring wheat cultivars associated with yield loss caused by a heat stress episode after anthesis. Journal Agronomy & Crop Science 201, 32–48.
Traits in spring wheat cultivars associated with yield loss caused by a heat stress episode after anthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXislWmtA%3D%3D&md5=7fd41ae465ccc21cef6c45588a29e510CAS |

Wardlaw I, Moncur L (1995) The response of wheat to high temperature following anthesis. I. The rate and duration of kernel filling. Functional Plant Biology 22, 391–397.

Wardlaw I, Wrigley C (1994) Heat tolerance in temperate cereals: an overview. Functional Plant Biology 21, 695–703.

Wardlaw I, Sofield I, Cartwright P (1980) Factors limiting the rate of dry matter accumulation in the grain of wheat grown at high temperature. Functional Plant Biology 7, 387–400.

Yemm E, Willis A (1954) The estimation of carbohydrates in plant extracts by anthrone. The Biochemical Journal 57, 508–514.
The estimation of carbohydrates in plant extracts by anthrone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2cXlvFOmtw%3D%3D&md5=51b32e5bf16c9fb78c2e5384c4ab834dCAS | 13181867PubMed |

Zahedi M, Jenner CF (2003) Analysis of effects in wheat of high temperature on grain filling attributes estimated from mathematical models of grain filling. The Journal of Agricultural Science 141, 203–212.
Analysis of effects in wheat of high temperature on grain filling attributes estimated from mathematical models of grain filling.Crossref | GoogleScholarGoogle Scholar |