Inhibition of rice germination by ustiloxin A involves alteration in carbon metabolism and amino acid utilization

Xiaoxiang Fu; Yu Jin; Matthew J Paul; Minxuan Yuan; Xingwei Liang; Ruqiang Cui; Yingjin Huang; Wenwen Peng; Xiaogui Liang

doi:10.3389/fpls.2023.1168985

Inhibition of rice germination by ustiloxin A involves alteration in carbon metabolism and amino acid utilization

Front Plant Sci. 2023 May 8:14:1168985. doi: 10.3389/fpls.2023.1168985. eCollection 2023.

Authors

Xiaoxiang Fu^{1

2

3}, Yu Jin², Matthew J Paul⁴, Minxuan Yuan¹, Xingwei Liang², Ruqiang Cui², Yingjin Huang², Wenwen Peng^{1

2}, Xiaogui Liang^{1

2

3}

Affiliations

¹ The Laboratory for Phytochemistry and Botanical Pesticides, College of Agriculture, Jiangxi Agricultural University, Nanchang, China.
² Key Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education/Jiangxi Province, Jiangxi Agricultural University, Nanchang, China.
³ College of Agronomy and Biotechnology, China Agricultural University, Beijing, China.
⁴ Plant Sciences, Rothamsted Research, Harpenden, United Kingdom.

Abstract

Ustiloxins are the main mycotoxin in rice false smut, a devastating disease caused by Ustilaginoidea virens. A typical phytotoxicity of ustiloxins is strong inhibition of seed germination, but the physiological mechanism is not clear. Here, we show that the inhibition of rice germination by ustiloxin A (UA) is dose-dependent. The sugar availability in UA-treated embryo was lower while the starch residue in endosperm was higher. The transcripts and metabolites responsive to typical UA treatment were investigated. The expression of several SWEET genes responsible for sugar transport in embryo was down-regulated by UA. Glycolysis and pentose phosphate processes in embryo were transcriptionally repressed. Most of the amino acids detected in endosperm and embryo were variously decreased. Ribosomal RNAs for growth were inhibited while the secondary metabolite salicylic acid was also decreased under UA. Hence, we propose that the inhibition of seed germination by UA involves the block of sugar transport from endosperm to embryo, leading to altered carbon metabolism and amino acid utilization in rice plants. Our analysis provides a framework for understanding of the molecular mechanisms of ustiloxins on rice growth and in pathogen infection.

Keywords: carbon metabolism; rice false smut; seed germination; sugar transport; ustiloxins.

Grants and funding

This work was supported by the National Natural Science Foundation of China (32160445), the grants from the Education Department Funds (GJJ180215), and the Natural Science Funds of Jiangxi Province (20202BABL215004, 20202BABL215008). We also acknowledge support from the earmarked fund for Innovation team of Jiangxi Agricultural University (JXAUCXTD002) and the National Undergraduate Training Program for Innovation and Entrepreneurship (202210410005). Support is acknowledged from the Designing Future Wheat Institute Strategic Programme to MJP (BB/P016855/1).