Regulatory network of the late-recruited primary decarboxylase C4NADP-ME in sugarcane

In agronomically important C4 grasses, efficient CO2 delivery to Rubisco is facilitated by NADP-malic enzyme (C4NADP-ME), which decarboxylates malate in bundle sheath cells. However, understanding the molecular regulation of the C4NADP-ME gene in sugarcane (Saccharum spp.) is hindered by its complex genetic background. Enzymatic activity assays demonstrated that decarboxylation in sugarcane Saccharum spontaneum predominantly relies on the NADP-ME pathway, similar to sorghum (Sorghum bicolor) and maize (Zea mays). Comparative genomics analysis revealed the recruitment of 8 core C4 shuttle genes, including C4NADP-ME (SsC4NADP-ME2), in the C4 pathway of sugarcane. Contrasting to sorghum and maize, the expression of SsC4NADP-ME2 in sugarcane is regulated by different transcription factors (TFs). We propose a gene regulatory network for SsC4NADP-ME2, involving candidate TFs identified through gene coexpression analysis and yeast 1-hybrid experiment. Among these, ABA INSENSITIVE5 (ABI5) was validated as the predominant regulator of SsC4NADP-ME2 expression, binding to a G-box within its promoter region. Interestingly, the core element ACGT within the regulatory G-box was conserved in sugarcane, sorghum, maize, and rice (Oryza sativa), suggesting an ancient regulatory code utilized in C4 photosynthesis. This study offers insights into SsC4NADP-ME2 regulation, crucial for optimizing sugarcane as a bioenergy crop.

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Journal
PLANT PHYSIOLOGY
Published
2024-09-14
DOI
https://doi.org/10.1093/plphys/kiae455
Citations
3
Primary Topic
Biochemical and biochemical processes
Type
article
Field-Weighted Citation Impact
1.16
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article

Regulatory network of the late-recruited primary decarboxylase C4NADP-ME in sugarcane

Wei Yao, Xin‐Guang Zhu, Xingtan Zhang, Shaoli Zhou et al.
3 citations
PLANT PHYSIOLOGY
Biochemical and biochemical processes
1.16
article

Regulatory network of the late-recruited primary decarboxylase C4NADP-ME in sugarcane

Wei Yao, Xin‐Guang Zhu, Xingtan Zhang, Shaoli Zhou, Huihong Shi, Ray Ming, Shenghua Xiao, Xiaomin Yu, Muqing Zhang, Kaixin Huang, Yuhong Lan, Xiuting Hua, Sehrish Akbar, Qingwu Jiang, Ming‐Ju Amy Lyu, Pinghua Li, Dongxu Zhao, Haibao Tang, Jisen Zhang, Zhen Li, Yuan Yuan, Jianping Wang, Qing Zhang, Yu Wang, Jia Liu, Gang Wang, Zhuang Gui, Yating Zhang
article en
3 citations

Abstract

In agronomically important C4 grasses, efficient CO2 delivery to Rubisco is facilitated by NADP-malic enzyme (C4NADP-ME), which decarboxylates malate in bundle sheath cells. However, understanding the molecular regulation of the C4NADP-ME gene in sugarcane (Saccharum spp.) is hindered by its complex genetic background. Enzymatic activity assays demonstrated that decarboxylation in sugarcane Saccharum spontaneum predominantly relies on the NADP-ME pathway, similar to sorghum (Sorghum bicolor) and maize (Zea mays). Comparative genomics analysis revealed the recruitment of 8 core C4 shuttle genes, including C4NADP-ME (SsC4NADP-ME2), in the C4 pathway of sugarcane. Contrasting to sorghum and maize, the expression of SsC4NADP-ME2 in sugarcane is regulated by different transcription factors (TFs). We propose a gene regulatory network for SsC4NADP-ME2, involving candidate TFs identified through gene coexpression analysis and yeast 1-hybrid experiment. Among these, ABA INSENSITIVE5 (ABI5) was validated as the predominant regulator of SsC4NADP-ME2 expression, binding to a G-box within its promoter region. Interestingly, the core element ACGT within the regulatory G-box was conserved in sugarcane, sorghum, maize, and rice (Oryza sativa), suggesting an ancient regulatory code utilized in C4 photosynthesis. This study offers insights into SsC4NADP-ME2 regulation, crucial for optimizing sugarcane as a bioenergy crop.

PLANT PHYSIOLOGYVol. 196(4)
Guangxi University (CN), University of Illinois Urbana-Champaign (US), University of Florida (US), Center for Excellence in Molecular Plant Sciences (CN), Fujian Agriculture and Forestry University (CN), Shandong Agricultural University (CN)
Openalex Percentile: Top 22%
Biochemical and biochemical processes
1.16
DOISourceOpenAlex
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