Oxidative Stress and Aberrant Programmed Cell Death Are Associated With Pollen Abortion in Isonuclear Alloplasmic Male-Sterile Wheat

Abstract

Cytoplasmic male sterility is crucial for the utilization of hybrid heterosis and it possibly occurs in parallel with tapetal programmed cell death (PCD) and oxidative metabolism responses. However, little is known about the mechanisms that underlie pollen abortion in wheat. Therefore, we obtained two isonuclear alloplasmic male sterile lines (IAMSLs) with Aegilops kotschyi and Ae. juvenalis cytoplasm. Compared with the maintainer line, cytochemical analyses of the anthers demonstrated that the IAMSLs exhibited anomalous tapetal PCD and organelles, with premature PCD in K87B1-706A and delayed PCD in Ju87B1-706A. We also found that the dynamic trends in reactive oxygen species (ROS) were consistent in these two IAMSLs during anther development and they were potentially associated with the initiation of tapetal PCD. In addition, the activities of ROS-scavenging enzymes increased rapidly, whereas non-enzymatic antioxidants were downregulated together with excess ROS production in IAMSLs. Real-time PCR analysis showed that the expression levels of superoxide dismutase, catalase, and ascorbate peroxidase genes, which encode important antioxidant enzymes, were significantly upregulated during early pollen development. Thus, we inferred that excessive ROS and the abnormal transcript levels of antioxidant enzyme genes disrupted the balance of the antioxidant system and the presence of excess ROS may have been related to aberrant tapetal PCD progression, thereby affecting the development of microspores and ultimately causing male sterility. These relationships between the mechanism of PCD and ROS metabolism provide new insights into the mechanisms responsible for abortive pollen in wheat.

Pollen development at high temperature and role of carbon and nitrogen metabolites

“…Similarly, chemical‐induced reduction of ROS accumulation in tobacco ( Nicotiana tabacum ) and tomato ( Solanum lycopersicum ) anthers resulted in delayed tapetum degradation and pollen abortion (Yu, Feng, et al, ). In contrast, when ROS accumulation is increased in anthers such as in the isonuclear alloplasmic male sterile wheat ( Triticum aestivum ) that harbours Aegilops kotschyi cytoplasm, tapetum degradation was observed at the tetrad stage and was followed by pollen abortion (Liu, Shi, Li, Zhang, & Song, ). Increased anther accumulation of ROS was also recently seen in cytoplasmic male sterile Brassica napus along with deficiency in antioxidant enzyme system (Du et al, ).…”

Comparative transcriptome analysis indicates conversion of stamens into pistil-like structures in male sterile wheat (Triticum aestivum L.) with Aegilops crassa cytoplasm

“…Compared with fertile wheat, physiological studies have shown that sterile wheat accumulates more H 2 O 2 and malondialdehyde (MDA), and the O 2− generation rate is higher [16,17]. Thus, we determined the O 2− generation rate as well as the H 2 O 2 and MDA contents during all of the anther developmental stages (Fig.…”

Comparative transcriptome analysis revealed the conversions of stamens into pistil-like structures in Aegilops crassa cytoplasmic male sterile wheat (Triticum aestivum)

“…Compared with the physiological research of fertile wheat, the previous research results showed that sterile wheat higher accumulation of H 2 O 2 and MDA and had a higher O 2− generation rate [16,17].…”

“…The input data of gene differential expression was read count data obtained in gene expression level analysis. First, the read count data was standardized by TMM (trimmed mean of M values) [16]. Then these genes were used for the different analysis.…”