Deciphering heat wave effects on wheat grain: focusing on the starch fraction

Rita Pereira; Diana Tomás; Manuela Silva

doi:10.3389/fpls.2024.1459283

Deciphering heat wave effects on wheat grain: focusing on the starch fraction

Front Plant Sci. 2024 Dec 4:15:1459283. doi: 10.3389/fpls.2024.1459283. eCollection 2024.

Authors

Rita Pereira^#¹, Diana Tomás^#², Manuela Silva^{2

3}

Affiliations

¹ Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, Lisboa, Portugal.
² LEAF-Linking Landscape, Environment, Agriculture and Food Research Center, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, Lisboa, Portugal.
³ Associate Laboratory TERRA, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, Lisboa, Portugal.

^# Contributed equally.

Abstract

Wheat is an essential staple food, and its production and grain quality are affected by extreme temperature events. These effects are even more relevant considering the increasing food demand for a growing world population and the predicted augmented frequency of heat waves. This study investigated the impact of simulated heat wave (HW) conditions imposed during grain filling on starch granule characteristics, endosperm ultrastructure, and transcriptomic modulation of genes involved in starch synthesis and degradation. All these evaluations were performed with four different genotypes, two commercial wheat varieties (Antequera and Bancal), and two traditional landraces (Ardito and Magueija). Starch granule size distribution and shape were significantly altered by HW treatment, revealing an increase of A-type granules in Ardito and an opposite effect in Magueija and Bancal, while Antequera remained stable. Analysis of the largest (LD) and smallest (SD) granule diameters also revealed genotype-specific changes, with Magueija showing a shift toward more spherical A-type granules after the HW treatment. Scanning electron microscopy confirmed alterations in endosperm morphology, including increased vitreousness in Bancal and substantial increase of endosperm cavities and grain size reduction in Magueija under HW stress. The transcriptomic analysis confirmed the stability of Antequera under HW, in contrast with the other genotypes where differential gene expression related to starch metabolism was detected. These effects were particularly severe in Magueija with the downregulation of genes encoding for enzymes involved in amylopectin synthesis (both starch synthases and starch-branching enzyme) and upregulation of α-amylase-encoding genes. These findings contribute to the understanding of heat stress effects on wheat grain quality, emphasize the importance of genetic diversity in HW responses, and suggest potential avenues for breeding climate-resilient wheat varieties.

Keywords: Lugol iodine; RNA sequencing; SEM; bread wheat; endosperm ultrastructure; high temperature; starch granules; transcription.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. DT was funded by a Fundação para a Ciência e a Tecnologia, Portugal (FCT), doctoral scholarship (SFRH/BD/93156/2013). This work was funded by national funds through FCT—Fundação para a Ciência e a Tecnologia, I.P., under the projects UIDB/04129/2020 of LEAF-Linking Landscape, Environment, Agriculture and Food, Research Unit and LA/P/0092/2020 of Associate Laboratory TERRA.