A high-resolution gene expression atlas links dedicated meristem genes to key architectural traits

Steffen Knauer; Marie Javelle; Lin Li; Xianran Li; Xiaoli Ma; Kokulapalan Wimalanathan; Sunita Kumari; Robyn Johnston; Samuel Leiboff; Robert Meeley; Patrick S. Schnable; Doreen Ware; Carolyn Lawrence-Dill; Jianming Yu; Gary J. Muehlbauer; Michael J. Scanlon; Marja C.P. Timmermans

doi:10.1101/gr.250878.119

A high-resolution gene expression atlas links dedicated meristem genes to key architectural traits

Steffen Knauer, Marie Javelle, Lin Li, Xianran Li, Xiaoli Ma, Kokulapalan Wimalanathan, Sunita Kumari, Robyn Johnston, Samuel Leiboff, Robert Meeley, Patrick S. Schnable, Doreen Ware, Carolyn Lawrence-Dill, Jianming Yu, Gary J. Muehlbauer, Michael J. Scanlon, Marja C.P. Timmermans

Agronomy and Plant Genetics

Research output: Contribution to journal › Article › peer-review

31 Scopus citations

Abstract

The shoot apical meristem (SAM) orchestrates the balance between stem cell proliferation and organ initiation essential for postembryonic shoot growth. Meristems show a striking diversity in shape and size. How this morphological diversity relates to variation in plant architecture and the molecular circuitries driving it are unclear. By generating a high-resolution gene expression atlas of the vegetative maize shoot apex, we show here that distinct sets of genes govern the regulation and identity of stem cells in maize versus Arabidopsis. Cell identities in the maize SAM reflect the combinatorial activity of transcription factors (TFs) that drive the preferential, differential expression of individual members within gene families functioning in a plethora of cellular processes. Subfunctionalization thus emerges as a fundamental feature underlying cell identity. Moreover, we show that adult plant characters are, to a significant degree, regulated by gene circuitries acting in the SAM, with natural variation modulating agronomically important architectural traits enriched specifically near dynamically expressed SAM genes and the TFs that regulate them. Besides unique mechanisms of maize stem cell regulation, our atlas thus identifies key new targets for crop improvement.

Original language	English (US)
Pages (from-to)	1962-1973
Number of pages	12
Journal	Genome research
Volume	29
Issue number	12
DOIs	https://doi.org/10.1101/gr.250878.119
State	Published - 2019

Bibliographical note

Funding Information:
We thank members of the Timmermans lab for their insightful feedback and helpful comments on the manuscript. We also thank Tim Mulligan, Sarah Vermylen, and Gert Huber for plant care. This work was supported by award IOS-1238142 and IOS-1127112 from the U.S. National Science Foundation Plant Genome Research Program. S.K. was supported by a research fellowship from the German Research Foundation (DFG, KN 1150/1-1); research in the Ware lab is further supported by the U.S. Department of Agriculture, Agricultural Research Service (USDA ARS) 58-8062-7-008 and in the Timmermans lab by an Alexander von Humboldt Professorship.

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© 2019 Knauer et al.

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Knauer, S., Javelle, M., Li, L., Li, X., Ma, X., Wimalanathan, K., Kumari, S., Johnston, R., Leiboff, S., Meeley, R., Schnable, P. S., Ware, D., Lawrence-Dill, C., Yu, J., Muehlbauer, G. J., Scanlon, M. J., & Timmermans, M. C. P. (2019). A high-resolution gene expression atlas links dedicated meristem genes to key architectural traits. Genome research, 29(12), 1962-1973. https://doi.org/10.1101/gr.250878.119

Knauer, S, Javelle, M, Li, L, Li, X, Ma, X, Wimalanathan, K, Kumari, S, Johnston, R, Leiboff, S, Meeley, R, Schnable, PS, Ware, D, Lawrence-Dill, C, Yu, J, Muehlbauer, GJ, Scanlon, MJ & Timmermans, MCP 2019, 'A high-resolution gene expression atlas links dedicated meristem genes to key architectural traits', Genome research, vol. 29, no. 12, pp. 1962-1973. https://doi.org/10.1101/gr.250878.119

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abstract = "The shoot apical meristem (SAM) orchestrates the balance between stem cell proliferation and organ initiation essential for postembryonic shoot growth. Meristems show a striking diversity in shape and size. How this morphological diversity relates to variation in plant architecture and the molecular circuitries driving it are unclear. By generating a high-resolution gene expression atlas of the vegetative maize shoot apex, we show here that distinct sets of genes govern the regulation and identity of stem cells in maize versus Arabidopsis. Cell identities in the maize SAM reflect the combinatorial activity of transcription factors (TFs) that drive the preferential, differential expression of individual members within gene families functioning in a plethora of cellular processes. Subfunctionalization thus emerges as a fundamental feature underlying cell identity. Moreover, we show that adult plant characters are, to a significant degree, regulated by gene circuitries acting in the SAM, with natural variation modulating agronomically important architectural traits enriched specifically near dynamically expressed SAM genes and the TFs that regulate them. Besides unique mechanisms of maize stem cell regulation, our atlas thus identifies key new targets for crop improvement.",

author = "Steffen Knauer and Marie Javelle and Lin Li and Xianran Li and Xiaoli Ma and Kokulapalan Wimalanathan and Sunita Kumari and Robyn Johnston and Samuel Leiboff and Robert Meeley and Schnable, {Patrick S.} and Doreen Ware and Carolyn Lawrence-Dill and Jianming Yu and Muehlbauer, {Gary J.} and Scanlon, {Michael J.} and Timmermans, {Marja C.P.}",

note = "Funding Information: We thank members of the Timmermans lab for their insightful feedback and helpful comments on the manuscript. We also thank Tim Mulligan, Sarah Vermylen, and Gert Huber for plant care. This work was supported by award IOS-1238142 and IOS-1127112 from the U.S. National Science Foundation Plant Genome Research Program. S.K. was supported by a research fellowship from the German Research Foundation (DFG, KN 1150/1-1); research in the Ware lab is further supported by the U.S. Department of Agriculture, Agricultural Research Service (USDA ARS) 58-8062-7-008 and in the Timmermans lab by an Alexander von Humboldt Professorship. Publisher Copyright: {\textcopyright} 2019 Knauer et al.",

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AU - Ma, Xiaoli

AU - Wimalanathan, Kokulapalan

AU - Kumari, Sunita

AU - Johnston, Robyn

AU - Leiboff, Samuel

AU - Meeley, Robert

AU - Schnable, Patrick S.

AU - Ware, Doreen

AU - Lawrence-Dill, Carolyn

AU - Yu, Jianming

AU - Muehlbauer, Gary J.

AU - Scanlon, Michael J.

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A high-resolution gene expression atlas links dedicated meristem genes to key architectural traits

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