INDETERMINATE1 autonomously regulates phosphate homeostasis upstream of the miR399-ZmPHO2signaling module in maize

Author:

Wang Xufeng123ORCID,Yuan Dan12ORCID,Liu Yanchun12ORCID,Liang Yameng4ORCID,He Juan12ORCID,Yang Xiaoyu125ORCID,Hang Runlai3ORCID,Jia Hong4ORCID,Mo Beixin1ORCID,Tian Feng4ORCID,Chen Xuemei3ORCID,Liu Lin1ORCID

Affiliation:

1. Guangdong Provincial Key Laboratory for Plant Epigenetics, Longhua Bioindustry and Innovation Research Institute, College of Life Sciences and Oceanography, Shenzhen University , Shenzhen, Guangdong 518060 , China

2. Key Laboratory of Optoelectronic Devices and Systems of Ministry of Education and Guangdong Province, College of Optoelectronic Engineering, Shenzhen University , Shenzhen, Guangdong 518060 , China

3. Department of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of California , Riverside, CA 92521 , USA

4. State Key Laboratory of Plant Physiology and Biochemistry, National Maize Improvement Center, Key Laboratory of Biology and Genetic Improvement of Maize (MOA), Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University , Beijing 100193 , China

5. College of Horticulture Science and Engineering, Shandong Agricultural University , Taian 271018 , China

Abstract

AbstractThe macronutrient phosphorus is essential for plant growth and development. Plants have evolved multiple strategies to increase the efficiency of phosphate (Pi) acquisition to protect themselves from Pi starvation. However, the crosstalk between Pi homeostasis and plant development remains to be explored. Here, we report that overexpressing microRNA399 (miR399) in maize (Zea mays) is associated with premature senescence after pollination. Knockout of ZmPHO2 (Phosphate 2), a miR399 target, resulted in a similar premature senescence phenotype. Strikingly, we discovered that INDETERMINATE1 (ID1), a floral transition regulator, inhibits the transcription of ZmMIR399 genes by directly binding to their promoters, alleviating the repression of ZmPHO2 by miR399 and ultimately contributing to the maintenance of Pi homeostasis in maize. Unlike ZmMIR399 genes, whose expression is induced by Pi deficiency, ID1 expression was independent of the external inorganic orthophosphate status, indicating that ID1 is an autonomous regulator of Pi homeostasis. Furthermore, we show that ZmPHO2 was under selection during maize domestication and cultivation, resulting in a more sensitive response to Pi starvation in temperate maize than in tropical maize. Our study reveals a direct functional link between Pi-deprivation sensing by the miR399-ZmPHO2 regulatory module and plant developmental regulation by ID1.

Publisher

Oxford University Press (OUP)

Subject

Cell Biology,Plant Science

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