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. 2022 Mar 25:13:828270.
doi: 10.3389/fpls.2022.828270. eCollection 2022.

Beta-Amylase and Phosphatidic Acid Involved in Recalcitrant Seed Germination of Chinese Chestnut

Yang Liu  1   2 , Yu Zhang  1 , Yi Zheng  3 , Xinghua Nie  1 , Yafeng Wang  1 , Wenjie Yu  1 , Shuchai Su  2 , Qingqin Cao  1 , Ling Qin  1 , Yu Xing  1
Affiliations

Beta-Amylase and Phosphatidic Acid Involved in Recalcitrant Seed Germination of Chinese Chestnut

Yang Liu et al. Front Plant Sci. .

Abstract

Chinese chestnut (Castanea mollissima), a species with recalcitrant seeds, is an important source of nuts and forest ecosystem services. The germination rate of recalcitrant seeds is low in natural habitats and decreases under conditions of desiccation and low temperature. The germination rate of cultivated Chinese chestnut seeds is significantly higher than that of wild seeds. To explore the reasons for the higher germination rate of cultivated seeds in Chinese chestnut, 113,524 structural variants (SVs) between the wild and cultivated Chinese chestnut genomes were detected through genome comparison. Genotyping these SVs in 60 Chinese chestnut accessions identified allele frequency changes during Chinese chestnut domestication, and some SVs are overlapping genes for controlling seed germination. Transcriptome analysis revealed downregulation of the abscisic acid synthesis genes and upregulation of the beta-amylase synthesis genes in strongly selected genes of cultivated seeds. On the other hand, hormone and enzyme activity assays indicated a decrease in endogenous ABA level and an increase in beta-amylase activity in cultivated seeds. These results shed light on the higher germination rate of cultivated seeds. Moreover, phosphatidic acid synthesis genes are highly expressed in seed germination stages of wild Chinese chestnut and may play a role in recalcitrant seed germination. These findings provide new insight into the regulation of wild seed germination and promote natural regeneration and succession in forest ecosystems.

Keywords: SVs; amylase; phosphatidic acid; recalcitrant seeds; seed germination.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Morphology and physiology of the seed germination process at different developmental stages in wild and cultivated Chinese chestnut. (A) Morphology of wild and cultivated Chinese chestnut seeds at different developmental stages of germination. S1: seed embryos after imbibition for 0 h; S2: seed embryos after imbibition for 3 h; S3: radicle emergence at 96 h for cultivated seeds and 216 h for wild seeds. (B) The seed germination rate of Chinese chestnut. * indicates a significant difference at P < 0.05.
FIGURE 2
FIGURE 2
SVs under selection during Chinese chestnut domestication and breeding. (A) PCA plots of wild and cultivated Chinese chestnut accessions. (B) Percentages of SVs with genotypes in different populations. (C) GO enrichment of genes with strongly selected SVs in Chinese chestnut. (D) KEGG enrichment of genes with strongly selected SVs in Chinese chestnut.
FIGURE 3
FIGURE 3
Strong selection of genes between wild and cultivated Chinese chestnut. (A) Genome-wide distribution of selective sweeps in Chinese chestnut. (B) FST, π, and XP-CLR values across the genomic regions of the ABA2, PLD1 and AMY1 genes. The dashed horizontal line represents the selection threshold (top 5% of the genome). Red dots denote the genes that are connected.
FIGURE 4
FIGURE 4
Selected amylase genes associated with the germination of Chinese chestnut seeds. (A) Seed germination-related gene expression profiles of Chinese chestnut, where * indicates a significant difference at P < 0.05. (B) Levels of endogenous hormones in Chinese chestnut at seed germination stage S3, where * indicates a significant difference at P < 0.05. (C) Alpha-amylase and beta-amylase activities in seed germination stages of wild and cultivated Chinese chestnut seeds; * indicates a significant difference at P < 0.05. (D) The allele frequencies of selected SVs in wild and cultivated Chinese chestnut. (E) The model of seed germination regulation by ABA synthesis pathway genes under strong selection in Chinese chestnut; * indicates the significance of the key genes.
FIGURE 5
FIGURE 5
Glycerophospholipid metabolism genes associated with the germination of Chinese chestnut seeds. (A) Model of the glycerophospholipid metabolism pathway in Chinese chestnut; * indicates significant key genes. (B) The glycerophospholipid metabolism gene expression profiles of Chinese chestnut, where * indicates a significant difference at P < 0.05. (C) Allele frequencies of selected SVs in wild and cultivated Chinese chestnut.
FIGURE 6
FIGURE 6
Model of the seed germination mechanism regulated by strongly selected genes in Chinese chestnut.
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