ROS accumulation-induced tapetal PCD timing changes leads to microspore abortion in cotton CMS lines

Abstract

Background Cytoplasmic male sterility (CMS) is the basis of heterosis exploitation. CMS has been used to hybrid production in cotton, but its molecular mechanism remains unclear. CMS is associated with advanced or delayed tapetal programmed cell death (PCD), and reactive oxygen species (ROS) may mediate this process. In this study, we obtained Jin A and Yamian A, two CMS lines with different cytoplasmic sources. Results Compared with maintainer Jin B, Jin A anthers showed advanced tapetal PCD with DNA fragmentation, producing excessive ROS which accumulated around the cell membrane, intercellular space and mitochondrial membrane. The activities of peroxidase (POD) and catalase (CAT) enzymes which can scavenge ROS were significantly decreased. However, Yamian A tapetal PCD was delayed with lower ROS content, and the activities of superoxide dismutase (SOD) and POD were higher than its maintainer. These differences in ROS scavenging enzyme activities may be caused by isoenzyme gene expressions. In addition, we found the excess ROS generated in Jin A mitochondria and ROS overflow from complex III might be the source in parallel with the reduction of ATP content. Conclusion ROS accumulation or abrogation were mainly caused by the joint action of ROS generation and scavenging enzyme activities transformation, which led to the abnormal progression of tapetal PCD, affected the development of microspores, and eventually contributed to male sterility. In Jin A, tapetal PCD in advance might be caused by mitochondrial ROS overproduction, accompanied by energy deficiency. The above studies will provide new insights into the cotton CMS and guide the follow-up research ideas.

Abnormal Calcium Accumulation and ROS Homeostasis-Induced Tapetal Programmed Cell Death Lead to Pollen Abortion of Petaloid-Type Cytoplasmic Male Sterility in Camellia oleifera

“…The activity of antioxidant enzymes in anthers is regulated by related genes. In the YamianA line in cotton, the expression trend of MnSOD was the same as SOD activity and the expression trend of CAT1 was the same as CAT [32]. In our study, the expression levels of CoPOD and CoCAT genes were uniformly upregulated in the early stage of HSP pollen development, but were lower than that in HS at the same stage, which was similar to the trend of enzyme activity.…”

“…In fact, the lack of antioxidant system in HSP led to the overproduction of ROS, thus upsetting the ROS balance. In cotton CMS line Jin A, the activity of POD and CAT in anthers was significantly reduced, and excess ROS was produced [32]. The soybean CMS line SXCMS5A also reported the same results with reduced anther ROS scavenging [47].…”

“…A standard solution of 1 mmol/mL hydrogen peroxide treated with the same procedure was used as a control. The absorbance value of the treated samples was measured at 415 nm wavelength, and the hydrogen peroxide content of fresh tissue weight was calculated [32].…”

“…For MDA measurement, the samples were mixed and ground in distilled water, a 0.5% (w/v) thiobarbituric acid solution with 20% trichloroacetic acid was added, and the samples were bathed in water at 100 • C for 10 min. The absorbance was determined at 450 nm, 532 nm, and 600 nm, and MDA content was calculated according to Zhang [32].…”

Ac-DEVD-CHO (caspase-3/DEVDase inhibitor) suppresses self-incompatibility–induced programmed cell death in the pollen tubes of petunia (Petunia hybrida E. Vilm.)

“…Many of them are morphologically described; however, the data on the underlying biochemical mechanisms are rather incomplete. The roles of some physiological factors, such as reactive oxygen species [ 42 ] and phytohormones [ 22 , 43 ] have been revealed. However, there are no doubts that caspases are ideal effectors for providing PCD [ 44 ].…”