Integrative transcriptome and metabolome analysis reveals the mechanisms of light-induced pigmentation in purple waxy maize

Yuan Lu; Yao Yu; Yanfang Xuan; Ayiguli Kari; Caixia Yang; Chenyu Wang; Chao Zhang; Wei Gu; Hui Wang; Yingxiong Hu; Pingdong Sun; Yuan Guan; Wenshuai Si; Bing Bai; Xuecai Zhang; Yunbi Xu; Boddupalli M Prasanna; Biao Shi; Hongjian Zheng

doi:10.3389/fpls.2023.1203284

Integrative transcriptome and metabolome analysis reveals the mechanisms of light-induced pigmentation in purple waxy maize

Front Plant Sci. 2023 Aug 15:14:1203284. doi: 10.3389/fpls.2023.1203284. eCollection 2023.

Authors

Yuan Lu^{1

2

3

4}, Yao Yu^{1

2

3

4}, Yanfang Xuan⁵, Ayiguli Kari^{1

2

3

4}, Caixia Yang^{1

2

3

4}, Chenyu Wang^{1

2

3

4}, Chao Zhang^{1

2

3

4}, Wei Gu^{1

2

3

4}, Hui Wang^{1

2

3

4}, Yingxiong Hu^{1

2

3

4}, Pingdong Sun^{1

2

3

4}, Yuan Guan^{1

2

3

4}, Wenshuai Si⁵, Bing Bai⁵, Xuecai Zhang⁶, Yunbi Xu^{2

6

7}, Boddupalli M Prasanna⁸, Biao Shi⁹, Hongjian Zheng^{1

2

3

4}

Affiliations

¹ Crop Breeding and Cultivation Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai, China.
² CIMMYT-China Specialty Maize Research Center, Shanghai Academy of Agricultural Sciences, Shanghai, China.
³ Shanghai Engineering Research Center of Specialty Maize, Shanghai Academy of Agricultural Sciences, Shanghai, China.
⁴ Key Laboratory of Germplasm Innovation and Genetic Improvement of Grain and Oil Crops (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Shanghai, China.
⁵ Institute for Agri-Food Standards and Testing Technology, Shanghai Academy of Agricultural Sciences, Shanghai, China.
⁶ International Maize and Wheat Improvement Center (CIMMYT), Texcoco, Mexico.
⁷ Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China.
⁸ International Maize and Wheat Improvement Center (CIMMYT), Nairobi, Kenya.
⁹ Shanghai Key Laboratory of Agricultural Genetics and Breeding, Shanghai, China.

Abstract

Introduction: Waxy maize, mainly consumed at the immature stage, is a staple and vegetable food in Asia. The pigmentation in the kernel of purple waxy maize enhances its nutritional and market values. Light, a critical environmental factor, affects anthocyanin biosynthesis and results in pigmentation in different parts of plants, including in the kernel. SWL502 is a light-sensitive waxy maize inbred line with purple kernel color, but the regulatory mechanism of pigmentation in the kernel resulting in purple color is still unknown.

Methods: In this study, cyanidin, peonidin, and pelargonidin were identified as the main anthocyanin components in SWL502, evaluated by the ultra-performance liquid chromatography (UPLC) method. Investigation of pigment accumulation in the kernel of SWL502 was performed at 12, 17, and 22 days after pollination (DAP) under both dark and light treatment conditions via transcriptome and metabolome analyses.

Results: Dark treatment affected genes and metabolites associated with metabolic pathways of amino acid, carbohydrate, lipid, and galactose, biosynthesis of phenylpropanoid and terpenoid backbone, and ABC transporters. The expression of anthocyanin biosynthesis genes, such as 4CL2, CHS, F3H, and UGT, was reduced under dark treatment. Dynamic changes were identified in genes and metabolites by time-series analysis. The genes and metabolites involved in photosynthesis and purine metabolism were altered in light treatment, and the expression of genes and metabolites associated with carotenoid biosynthesis, sphingolipid metabolism, MAPK signaling pathway, and plant hormone signal transduction pathway were induced by dark treatment. Light treatment increased the expression level of major transcription factors such as LRL1, myc7, bHLH125, PIF1, BH093, PIL5, MYBS1, and BH074 in purple waxy maize kernels, while dark treatment greatly promoted the expression level of transcription factors RVE6, MYB4, MY1R1, and MYB145.

Discussion: This study is the first report to investigate the effects of light on waxy maize kernel pigmentation and the underlying mechanism at both transcriptome and metabolome levels, and the results from this study are valuable for future research to better understand the effects of light on the regulation of plant growth.

Keywords: anthocyanin; light; metabolomics; transcriptomics; waxy maize.

Grants and funding

This work was sponsored by the Shanghai Rising-Star Program (Grant Number: 23QB1403100), Shanghai Agriculture Applied Technology Development Program, China (Grant Number: 2022-02-08-00-12-F01200), and Youth Science and Technology Personnel of Shanghai Academy of Agricultural Sciences (Grant Number: ZP22121).