Regulators of early maize leaf development inferred from transcriptomes of laser capture microdissection (LCM)-isolated embryonic leaf cells

Author:

Liu Wen-Yu1,Yu Chun-Ping1ORCID,Chang Chao-Kang1ORCID,Chen Hsiang-June1,Li Meng-Yun1,Chen Yi-Hua1,Shiu Shin-Han23ORCID,Ku Maurice S. B.45,Tu Shih-Long6,Lu Mei-Yeh Jade1,Li Wen-Hsiung17

Affiliation:

1. Biodiversity Research Center, Academia Sinica, Taipei 115, Taiwan

2. Department of Plant Biology, Michigan State University, East Lansing, MI 48824

3. Department of Computational Mathematics, Science, and Engineering, Michigan State University, East Lansing, MI 48824

4. Department of Bioagricultural Science, National Chiayi University, Chiayi 600, Taiwan

5. School of Biological Sciences, Washington State University, Pullman, WA 99164

6. Institute of Plant and Microbial Biology, Academia Sinica, Taipei 115, Taiwan

7. Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637

Abstract

The superior photosynthetic efficiency of C4leaves over C3leaves is owing to their unique Kranz anatomy, in which the vein is surrounded by one layer of bundle sheath (BS) cells and one layer of mesophyll (M) cells. Kranz anatomy development starts from three contiguous ground meristem (GM) cells, but its regulators and underlying molecular mechanism are largely unknown. To identify the regulators, we obtained the transcriptomes of 11 maize embryonic leaf cell types from five stages of pre-Kranz cells starting from median GM cells and six stages of pre-M cells starting from undifferentiated cells. Principal component and clustering analyses of transcriptomic data revealed rapid pre-Kranz cell differentiation in the first two stages but slow differentiation in the last three stages, suggesting early Kranz cell fate determination. In contrast, pre-M cells exhibit a more prolonged transcriptional differentiation process. Differential gene expression and coexpression analyses identified gene coexpression modules, one of which included 3 auxin transporter and 18 transcription factor (TF) genes, including known regulators of Kranz anatomy and/or vascular development. In situ hybridization of 11 TF genes validated their expression in early Kranz development. We determined the binding motifs of 15 TFs, predicted TF target gene relationships among the 18 TF and 3 auxin transporter genes, and validated 67 predictions by electrophoresis mobility shift assay. From these data, we constructed a gene regulatory network for Kranz development. Our study sheds light on the regulation of early maize leaf development and provides candidate leaf development regulators for future study.

Funder

Academia Sinica

US National Science Foundation

U.S. Department of Energy

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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