Modified expression of TaCYP78A5 enhances grain weight with yield potential by accumulating auxin in wheat (Triticum aestivum L.)

Abstract

Summary Increasing grain yield has always been the primary goal of crop breeding. KLUH/CYP78A5 has been shown to affect seed size in several plant species, but the relevant molecular mechanism is still unclear and there are no reports of this gene contributing to yield. Here, we demonstrate that modified expression of TaCYP78A5 can enhance wheat grain weight and grain yield per plant by accumulating auxin. TaCYP78A5 is highly expressed in maternal tissues, including ovary and seed coat during wheat development. The constitutive overexpression of TaCYP78A5 leads to significantly increased seed size and weight but not grain yield per plant due to the strengthening of apical dominance. However, localized overexpression of TaCYP78A5 in maternal integument enhances grain weight and grain yield per plant by 4.3%–18.8% and 9.6%–14.7%, respectively, in field trials. Transcriptome and hormone metabolome analyses reveal that TaCYP78A5 participates in auxin synthesis pathway and promotes auxin accumulation and cell wall remodelling in ovary. Phenotype investigation and cytological observation show that localized overexpression of TaCYP78A5 in ovary results in delayed flowering and prolonged proliferation of maternal integument cells, which promote grain enlargement. Moreover, naturally occurring variations in the promoter of TaCYP78A5‐2A contribute to thousand‐grain weight (TGW) and grain yield per plant of wheat;TaCYP78A5‐2A haplotype Ap‐HapII with higher activity is favourable for improving grain weight and grain yield per plant and has been positively selected in wheat breeding. Then, a functional marker of TaCYP78A5 haplotype Ap‐HapII is developed for marker‐assisted selection in wheat grain and yield improvement.

Overexpression of TaLBD16-4D alters plant architecture and heading date in transgenic wheat

“…Auxin is also involved in the flowering pathway in strawberry through its regulation of auxin response factor4 ( ARF4 ) expression, which can bind to the promoters of the floral meristem identity genes APETALA1 ( AP1 ) and FRUITFULL ( FUL ), inducing their expression ( Dong et al., 2021 ). The involvement of TaCYP78A5 in auxin synthesis pathway and auxin accumulation contributes to the delayed heading and flowering in wheat ( Guo et al., 2022 ). However, it has not been reported whether there are correlations between the key flowering regulators and auxin in wheat.…”

A lineage‐specific arginine in POS1 is required for fruit size control in Physaleae (Solanaceae) via gene co‐option

“…IAA9 is a negative auxin response regulator belonging to the auxin (Aux)/IAA transcription factor gene family, and Aux/IAA proteins play a role in fruit development in tomato, i.e., by regulating parthenocarpic fruit and fruit size (Su et al., 2014; Wang et al., 2005). Furthermore, CYP79B2 and CYP79B3 in Arabidopsis catalyze the first step of tryptophan‐dependent IAA biosynthesis and convert tryptophan to indole‐3‐acetaldoxime, a precursor to IAA (Hull et al., 2000), and several cytochrome P450 genes from crops, such as wheat ( Triticum aestivum ) TaCYP78A5 , regulate auxin accumulation (Guo et al., 2022), implying the potential role of CYP85A3 in IAA synthesis. Therefore, POS1 could directly or indirectly regulate CYP85A3 and IAA9 and integrate into the cell expansion regulatory pathways, thus regulating fruit size (Figure 9a).…”

“…The constitutive expression of PtCYP85A3 increases the endogenous BR levels and significantly promotes growth and biomass production in both transgenic tomato and poplar P. floridana (Jin et al, 2017). More interestingly, CYP85A homologous genes, including soybean (Glycine max) CYP85A2, tomato FW3.2 (CYP78A), Arabidopsis KLUH (CYP78A5), and the CYP78A class genes in various plants and crops, are all associated with larger fruits, seeds, and yield-related traits (Wang et al, 2008;Adamski et al, 2009;Fang et al, 2012;Chakrabarti et al, 2013;Nagasawa et al, 2013;Monforte et al, 2014;Wang et al, 2015b;Qi et al, 2017;Guo et al, 2022;Yang et al, 2021). Significant downregulation of CYP85A3 in the POS1-edited lines was due to either loss of direct POS1 regulation or PIPs-BRI-BZR regulation (Figure 9a), indicating the involvement of POS1 in the BR biosynthetic and signal transduction pathway.…”

“…IAA9 is a negative auxin response regulator belonging to the auxin (Aux)/IAA transcription factor gene family, and Aux/IAA proteins play a role in fruit development in tomato, i.e., by regulating parthenocarpic fruit and fruit size (Su et al, 2014;Wang et al, 2005). Furthermore, CYP79B2 and CYP79B3 in Arabidopsis catalyze the first step of tryptophan-dependent IAA biosynthesis and convert tryptophan to indole-3-acetaldoxime, a precursor to IAA (Hull et al, 2000), and several cytochrome P450 genes from crops, such as wheat (Triticum aestivum) TaCYP78A5, regulate auxin accumulation (Guo et al, 2022) IAA9 and integrate into the cell expansion regulatory pathways, thus regulating fruit size (Figure 9a). With further observations of POS1-like responses to different hormones at different levels, we thus conclude that the functions of POS1 in fruit development might be fulfilled via the coordination of multiple hormone-related pathways, such as the IAA and BR pathways.…”

Treatment of Winter Wheat (Triticum aestivum L.) Seeds with Electromagnetic Field Influences Germination and Phytohormone Balance Depending on Seed Size

“…The size and quantity of seeds are important from an evolutionary point of view for the continuation of plant species. Seed size is genetically regulated and is a result of three different growth programs of the diploid embryo, the triploid endosperm, and the diploid maternal ovule [1,2]. Furthermore, epigenetic and environmental factors are also involved in seed development and affect the final agricultural yield [3].…”