Abstract

Leaves of C4 crops usually have higher radiation, water and nitrogen use efficiencies compared to the C3 species. Engineering C4 traits into C3 crops has been proposed as one of the most promising ways to repeal the biomass yield ceiling. To better understand the function of C4 photosynthesis, and to identify candidate genes that are associated with the C4 pathways, a comparative transcription network analysis was conducted on leaf developmental gradients of three C4 species including maize, green foxtail and sorghum and one C3 species, rice. By combining the methods of gene co-expression and differentially co-expression networks, we identified a total of 128 C4 specific genes. Besides the classic C4 shuttle genes, a new set of genes associated with light reaction, starch and sucrose metabolism, metabolites transportation, as well as transcription regulation, were identified as involved in C4 photosynthesis. These findings will provide important insights into the differential gene regulation between C3 and C4 species, and a good genetic resource for establishing C4 pathways in C3 crops.

Highlights

  • With growing population and increasing urbanization, humanity faces a looming food crisis, which to prevent, will require yields to be increased by at least 50% over the 40 years [1, 2]

  • Orthologues of genes encoding classic C4 enzymes preexisted in their C3 ancestors but are usually lowly expressed in C3 plants, while in C4 plants these genes are highly expressed and co-regulated by multiple stimuli, e.g., light [5, 9]; (2) Many proteins, encoded by multi-gene families and thought to fulfill housekeeping functions in C3 species [7, 9], are recruited into the C4 pathway after a neo-function is acquired for the C4 paralog [10], which may change its gene expression pattern [11]; (3) C4 genes are often expressed in a cell-type specific manner, i.e. bundle sheath (BS) or mesophyll (ME) cells

  • C4 photosynthesis is a complex metabolic pathway that relies on tight collaboration of many enzymes

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Summary

Introduction

With growing population and increasing urbanization, humanity faces a looming food crisis, which to prevent, will require yields to be increased by at least 50% over the 40 years [1, 2]. Orthologues of genes encoding classic C4 enzymes preexisted in their C3 ancestors but are usually lowly expressed in C3 plants, while in C4 plants these genes are highly expressed and co-regulated by multiple stimuli, e.g., light [5, 9]; (2) Many proteins, encoded by multi-gene families and thought to fulfill housekeeping functions in C3 species [7, 9], are recruited into the C4 pathway after a neo-function is acquired for the C4 paralog [10], which may change its gene expression pattern [11]; (3) C4 genes are often expressed in a cell-type specific manner, i.e. bundle sheath (BS) or mesophyll (ME) cells. These characteristics could be exploited to identify novel C4 genes as well as their regulatory networks, which in practice could provide guidance for strategies of establishing the C4 cycle in C3 plants, e.g., by transferring a group of genes instead of a single gene into C3 crops [5]

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