Progressive meristem and single-cell transcriptomes reveal the regulatory mechanisms underlying maize inflorescence development and sex differentiation

• Published in: Molecular plant Vol. 17; no. 7; pp. 1019 - 1037
• Main Authors: Sun, Yonghao, Dong, Liang, Kang, Lu, Zhong, Wanshun, Jackson, David, Yang, Fang
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 01.07.2024
• Subjects: floral organ; Gene Expression Regulation, Plant; inflorescence; Inflorescence - genetics; Inflorescence - growth & development; Inflorescence - metabolism; maize; Meristem - genetics; Meristem - growth & development; Meristem - metabolism; Plant Proteins - genetics; Plant Proteins - metabolism; RNA-binding protein; sex differentiation; Sex Differentiation - genetics; Single-Cell Analysis; single-cell RNA sequencing; Transcriptome - genetics; Zea mays - genetics; Zea mays - growth & development; Zea mays - metabolism; single-cell RNA sequencing; floral organ; sex differentiation; RNA-binding protein; maize; inflorescence
• ISSN: 1674-2052; 1752-9867; 1752-9867
• DOI: 10.1016/j.molp.2024.06.007

Maize develops separate ear and tassel inflorescences with initially similar morphology but ultimately different architecture and sexuality. The detailed regulatory mechanisms underlying these changes still remain largely unclear. In this study, through analyzing the time-course meristem transcriptomes and floret single-cell transcriptomes of ear and tassel, we revealed the regulatory dynamics and pathways underlying inflorescence development and sex differentiation. We identified 16 diverse gene clusters with differential spatiotemporal expression patterns and revealed biased regulation of redox, programmed cell death, and hormone signals during meristem differentiation between ear and tassel. Notably, based on their dynamic expression patterns, we revealed the roles of two RNA-binding proteins in regulating inflorescence meristem activity and axillary meristem formation. Moreover, using the transcriptional profiles of 53 910 single cells, we uncovered the cellular heterogeneity between ear and tassel florets. We found that multiple signals associated with either enhanced cell death or reduced growth are responsible for tassel pistil suppression, while part of the gibberellic acid signal may act non-cell-autonomously to regulate ear stamen arrest during sex differentiation. We further showed that the pistil-protection gene SILKLESS 1 (SK1) functions antagonistically to the known pistil-suppression genes through regulating common molecular pathways, and constructed a regulatory network for pistil-fate determination. Collectively, our study provides a deep understanding of the regulatory mechanisms underlying inflorescence development and sex differentiation in maize, laying the foundation for identifying new regulators and pathways for maize hybrid breeding and improvement. This study explores meristem transcriptomes and floret single-cell transcriptomes in maize ear and tassel, revealing the molecular features and pathways underlying inflorescence development and sex differentiation. Key findings include the roles of two RNA-binding proteins in inflorescence development, several major signals regulating sex differentiation, and the model for pistil-fate determination.