Deficiency of rice hexokinase HXK5 impairs synthesis and utilization of starch in pollen grains and causes male sterility

Lee, Sang‐Kyu; Kim, Hyun-Bi; Cho, Jung‐Il; Nguyen, Cong Danh; Moon, Sunok; Park, Jeong Eun; Park, Hye Rang; Huh, Jin Hoe; Jung, Kyungsook; Guiderdoni, Emmanuel; Jeon, Jong‐Seong

doi:10.1093/jxb/erz436

Cited by 33 publications

(33 citation statements)

References 53 publications

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“…OsHXK6 and RF6 protein form a complex inside mitochondria which is capable of cleaving atp6-orfH79 transcript at nucleotide 1,238, avoiding orfH79 mRNA from its translation and therefore reestablishing pollen fertility ( Huang et al, 2015 ). Similarly, OsHXK5 deficiency causes male sterility, however, the expression of a non-catalytic version of this protein, OsHXK5G113D, is not able to rescue the male-sterile phenotype ( Lee et al, 2019 ).…”

Section: Hexokinases Moonlighting Functions In Diverse Life Kingdomsmentioning

confidence: 99%

“…Although OsHXK5 is also capable of rescuing the rice plant from pollen sterility, it may not follow the same mechanism that OsHXK6 does. The fact that pollen from plants lacking OshHXK5 show reduced hexokinase activity and the catalytic inactive protein, OsHXK5G113D, does not restore fertility, may indicate that this additional activity relies on the hexokinase activity rather than on the sugar sensing ability ( Lee et al, 2019 ).…”

Section: Hexokinases Moonlighting Functions In Diverse Life Kingdomsmentioning

confidence: 99%

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Moonlighting Proteins: The Case of the Hexokinases

Rodríguez-Saavedra

Morgado-Martínez

Burgos-Palacios

et al. 2021

Front. Mol. Biosci.

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Moonlighting proteins are defined as proteins with two or more functions that are unrelated and independent to each other, so that inactivation of one of them should not affect the second one and vice versa. Intriguingly, all the glycolytic enzymes are described as moonlighting proteins in some organisms. Hexokinase (HXK) is a critical enzyme in the glycolytic pathway and displays a wide range of functions in different organisms such as fungi, parasites, mammals, and plants. This review discusses HXKs moonlighting functions in depth since they have a profound impact on the responses to nutritional, environmental, and disease challenges. HXKs’ activities can be as diverse as performing metabolic activities, as a gene repressor complexing with other proteins, as protein kinase, as immune receptor and regulating processes like autophagy, programmed cell death or immune system responses. However, most of those functions are particular for some organisms while the most common moonlighting HXK function in several kingdoms is being a glucose sensor. In this review, we also analyze how different regulation mechanisms cause HXK to change its subcellular localization, oligomeric or conformational state, the response to substrate and product concentration, and its interactions with membrane, proteins, or RNA, all of which might impact the HXK moonlighting functions.

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Section: Hexokinases Moonlighting Functions In Diverse Life Kingdomsmentioning

confidence: 99%

Section: Hexokinases Moonlighting Functions In Diverse Life Kingdomsmentioning

confidence: 99%

Moonlighting Proteins: The Case of the Hexokinases

Rodríguez-Saavedra

Morgado-Martínez

Burgos-Palacios

et al. 2021

Front. Mol. Biosci.

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“…It plays an important role in metabolism, glucose signal transduction, and phosphorylation of glucose and fructose [34]. HXKs constitute a class of multifunctional proteins that play an important role in promoting germination, inhibiting seedling formation under high glucose concentrations, promoting vegetative growth and flowering, restoring fertility, and transducing senescence signals [32,[35][36][37][38][39][40][41]. Therefore, by combining the biochemical characteristics, localization, and sensing ability of HXKs with other sugar-sensitive pathways, researchers can increase plant productivity [35].…”

Section: Introductionmentioning

confidence: 99%

Improving the Rice Photosynthetic Efficiency and Yield by Editing OsHXK1 via CRISPR/Cas9 System

Zheng

et al. 2021

IJMS

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Rice (Oryza sativa L.) is an important food crop species in China. Cultivating high-yielding rice varieties that have a high photosynthetic efficiency is an important goal of rice breeding in China. In recent years, due to the continual innovation of molecular breeding methods, many excellent genes have been applied in rice breeding, which is highly important for increasing rice yields. In this paper, the hexokinase gene OsHXK1 was knocked out via the CRISPR/Cas9 gene-editing method in the indica rice varieties Huanghuazhan, Meixiangzhan, and Wushansimiao, and OsHXK1-CRISPR/Cas9 lines were obtained. According to the results of a phenotypic analysis and agronomic trait statistics, the OsHXK1-CRISPR/Cas9 plants presented increased light saturation points, stomatal conductance, light tolerance, photosynthetic products, and rice yields. Moreover, transcriptome analysis showed that the expression of photosynthesis-related genes significantly increased. Taken together, our results revealed that knocking out OsHXK1 via the CRISPR/Cas9 gene-editing method could effectively lead to the cultivation of high-photosynthetic efficiency and high-yielding rice varieties. They also revealed the important roles of OsHXK1 in the regulation of rice yield and photosynthesis.

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“…Only a few genes controlling the synthesis of starch have been characterized in rice. The rice gene hexokinase5 OsHXK5 is essential for hexokinase activity during the pollen maturation phase, and hxk5 mutants display an upregulation of HXK5 at this stage, which impairs starch biosynthesis and, consequently, pollen tube formation, resulting in complete male sterility (Lee et al, 2020). Similarly, mutations in the plastidic phosphoglucomutase OspPGM and the ADP-glucose pyrophosphorylase OsAGPL4 genes lead to an upregulation of both genes during pollen maturation, which also affects starch biosynthesis and causes male sterility, as the pollen fails to germinate (Lee et al, 2016).…”

Section: Polysaccharide Metabolismmentioning

confidence: 99%

Exploiting Genic Male Sterility in Rice: From Molecular Dissection to Breeding Applications

et al. 2021

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Rice (Oryza sativa L.) occupies a very salient and indispensable status among cereal crops, as its vast production is used to feed nearly half of the world’s population. Male sterile plants are the fundamental breeding materials needed for specific propagation in order to meet the elevated current food demands. The development of the rice varieties with desired traits has become the ultimate need of the time. Genic male sterility is a predominant system that is vastly deployed and exploited for crop improvement. Hence, the identification of new genetic elements and the cognizance of the underlying regulatory networks affecting male sterility in rice are crucial to harness heterosis and ensure global food security. Over the years, a variety of genomics studies have uncovered numerous mechanisms regulating male sterility in rice, which provided a deeper and wider understanding on the complex molecular basis of anther and pollen development. The recent advances in genomics and the emergence of multiple biotechnological methods have revolutionized the field of rice breeding. In this review, we have briefly documented the recent evolution, exploration, and exploitation of genic male sterility to the improvement of rice crop production. Furthermore, this review describes future perspectives with focus on state-of-the-art developments in the engineering of male sterility to overcome issues associated with male sterility-mediated rice breeding to address the current challenges. Finally, we provide our perspectives on diversified studies regarding the identification and characterization of genic male sterility genes, the development of new biotechnology-based male sterility systems, and their integrated applications for hybrid rice breeding.

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Deficiency of rice hexokinase HXK5 impairs synthesis and utilization of starch in pollen grains and causes male sterility

Abstract: Analysis of rice hexokinase hxk5 mutants reveals that the function of OsHXK5 in starch biosynthesis and utilization is essential for normal pollen development, germination, and tube growth.

Cited by 33 publications

References 53 publications

Moonlighting Proteins: The Case of the Hexokinases

Moonlighting Proteins: The Case of the Hexokinases

Improving the Rice Photosynthetic Efficiency and Yield by Editing OsHXK1 via CRISPR/Cas9 System

Exploiting Genic Male Sterility in Rice: From Molecular Dissection to Breeding Applications

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