Rice myo‐inositol‐3‐phosphate synthase 2 (RINO2) alleviates heat injury‐induced impairment in pollen germination and tube growth by modulating Ca2+ signaling and actin filament cytoskeleton

SUMMARY Low phytic acid (lpa) crop is considered as an effective strategy to improve crop nutritional quality, but a substantial decrease in phytic acid (PA) usually has negative effect on agronomic performance and its response to environment adversities. Myo‐inositol‐3‐phosphate synthase (MIPS) is...

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Published in:The Plant journal : for cell and molecular biology 2024-07, Vol.119 (2), p.861-878
Main Authors: Zhou, Lujian, Asad, Muhammad‐Asad‐Ullah, Guan, Xianyue, Pan, Gang, Zhang, Yan, Cheng, Fangmin
Format: Article
Language:English
Subjects:
Actin
Biosynthesis
Calcium ions
Calcium signalling
Crops
Cytoskeleton
Fertility
Genotypes
Germination
Grain
Heat
Heat stress
Heat tolerance
High temperature
Injury prevention
Inositols
MIPS gene
Mutants
Nutritive value
Phosphatidylinositol
Phytic acid
Pollen
pollen germination
Pollen tubes
Rice
Rice (Oryza sativa L.)
Rice myo‐inositol‐3‐phosphate synthase (RINO)
spikelet fertility
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Summary:SUMMARY Low phytic acid (lpa) crop is considered as an effective strategy to improve crop nutritional quality, but a substantial decrease in phytic acid (PA) usually has negative effect on agronomic performance and its response to environment adversities. Myo‐inositol‐3‐phosphate synthase (MIPS) is the rate‐limiting enzyme in PA biosynthesis pathway, and regarded as the prime target for engineering lpa crop. In this paper, the rice MIPS gene (RINO2) knockout mutants and its wild type were performed to investigate the genotype‐dependent alteration in the heat injury‐induced spikelet fertility and its underlying mechanism for rice plants being imposed to heat stress at anthesis. Results indicated that RINO2 knockout significantly enhanced the susceptibility of rice spikelet fertility to heat injury, due to the severely exacerbated obstacles in pollen germination and pollen tube growth in pistil for RINO2 knockout under high temperature (HT) at anthesis. The loss of RINO2 function caused a marked reduction in inositol and phosphatidylinositol derivative concentrations in the HT‐stressed pollen grains, which resulted in the strikingly lower content of phosphatidylinositol 4,5‐diphosphate (PI (4,5) P2) in germinating pollen grain and pollen tube. The insufficient supply of PI (4,5) P2 in the HT‐stressed pollen grains disrupted normal Ca2+ gradient in the apical region of pollen tubes and actin filament cytoskeleton in growing pollen tubes. The severely repressed biosynthesis of PI (4,5) P2 was among the regulatory switch steps leading to the impaired pollen germination and deformed pollen tube growth for the HT‐stressed pollens of RINO2 knockout mutants. Significance Statement For engineering lpa rice, the knockout of RINO2 significantly enhanced susceptibility of spikelet fertility to heat injury at anthesis, which was mostly ascribed to the heat injury‐induced obstacle in pollen germination and pollen tube growth. High temperature significantly reduced the concentrations of inositol and PI (4,5) P2 concentration in pollen grains, this occurrence was strongly responsible for the disorder Ca2+ gradient and actin filament cytoskeleton in growing pollen tubes. These findings provide new understanding for the regulatory mechanism by which the loss of RINO2 function negatively affects pollen germination and pollen tube growth in response to HT exposure at anthesis.
ISSN:0960-7412
1365-313X
1365-313X
DOI:10.1111/tpj.16802