Comparative Transcriptome Analysis Reveals the Cause for Accumulation of Reactive Oxygen Species During Pollen Abortion in Cytoplasmic Male-Sterile Kenaf Line 722HA.

Zheng Zheng,Wang Wang,Chen Chen,Liao Liao,Liu Liu,Zhou Zhou

doi:10.3390/ijms20215515

Abstract

Cytoplasmic male sterility (CMS) is a maternally inherited trait used for hybrid production in plants, a novel kenaf CMS line 722HA was derived from the thermo-sensitive male-sterile mutant ‘HMS’ by recurrent backcrossing with 722HB. The line 722HA has great potential for hybrid breeding in kenaf. However, the underlying molecular mechanism that controls pollen abortion in 722HA remains unclear, thus limiting the full utilization of this line. To understand the possible mechanism governing pollen abortion in 722HA, cytological, transcriptomic, and biochemical analyses were carried out to compare the CMS line 722HA and its maintainer line 722HB. Cytological observations of the microspore development revealed premature degradation of the tapetum at the mononuclear stage, which resulted in pollen dysfunction. The k-means clustering analysis of differentially expressed genes (DEGs) revealed that these genes are related to processes associated with the accumulation of reactive oxygen species (ROS), including electron transport chain, F1F0-ATPase proton transport, positive regulation of superoxide dismutase (SOD), hydrogen peroxide catabolic, and oxidation-reduction. Biochemical analysis indicated that ROS-scavenging capability was lower in 722HA than in 722HB, resulting in an accumulation of excess ROS, which is consistent with the transcriptome results. Taken together, these results demonstrate that excessive ROS accumulation may affect the normal development of microspores. Our study provides new insight into the molecular mechanism of pollen abortion in 722HA and will promote further studies of kenaf hybrids.

Highlights

Cytoplasmic male sterility (CMS), in which a maternally inherited trait causes dysfunctional pollen, is a natural phenomenon that widely exists among higher plants
In the wheat CMS line U87B1-706A, delayed tapetal programmed cell death (PCD) and organelle disorder phenotype are present in the early mononuclear stage, and shrunken microspores and disordered extracellular structure occur in the late mononuclear stage [27]
Ubiquinol-cytochrome-c reductase (Complex III) exhibited sustained levels of low expression during the development of microspores in 722HA (Cluster 6). These results indicated that the low expression of these genes in 722HA lead to blockage of the electron transport chain, after which the electrons directly combined with oxygen molecules to produce excessive reactive oxygen species (ROS)

Summary

Introduction

Cytoplasmic male sterility (CMS), in which a maternally inherited trait causes dysfunctional pollen, is a natural phenomenon that widely exists among higher plants. The discovery and utilization of plant CMS have produced excellent germplasm resources for increase in crop yield, improvement of quality, and disease resistance. The discovery and utilization of cytoplasmic male-sterile kenaf plants can significantly improve yield, quality, and resistance, supporting the practical value of kenaf breeding [8,9,10]. In the past few decades, several natural cytoplasmic male-sterile kenaf mutants have been found [11,12,13] and have been used for the production of kenaf three-line hybrids. To date, the molecular regulatory mechanism controlling pollen abortion remains unknown, which has limited the widespread use of kenaf CMS line 722HA in hybrid production, so far

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Discussion

Conclusion