Reactive oxygen species mediate tapetal programmed cell death in tobacco and tomato

Abstract

BackgroundHybrid vigor is highly valued in the agricultural industry. Male sterility is an important trait for crop breeding. Pollen development is under strict control of both gametophytic and sporophytic factors, and defects in this process can result in male sterility. Both in the dicot Arabidopsis and in the moncot rice, proper timing of programmed cell death (PCD) in the tapetum ensures pollen development. Dynamic ROS levels have been reported to control tapetal PCD, and thus pollen development, in Arabidopsis and rice. However, it was unclear whether it is evolutionarily conserved, as only those two distantly related species were studied.ResultsHere, we performed histological analyses of anther development of two economically important dicot species, tobacco and tomato. We identified the same ROS amplitude during anther development in these two species and found that dynamic ROS levels correlate with the initiation and progression of tapetal PCD. We further showed that manipulating ROS levels during anther development severely impaired pollen development, resulting in partial male sterility. Finally, real-time quantitative PCR showed that several tobacco and tomato RBOHs, encoding NADPH oxidases, are preferentially expressed in anthers.ConclusionThis study demonstrated evolutionarily conserved ROS amplitude during anther development by examining two commercially important crop species in the Solanaceae. Manipulating ROS amplitude through genetic interference of RBOHs therefore may provide a practical way to generate male sterile plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-017-1025-3) contains supplementary material, which is available to authorized users.

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

“…The anthers were then collected in the tetrad stage, early uninucleate stage, late uninucleate stage, binucleate stage, and trinucleate stage. The total DNA was isolated from the DPI-treated anthers in different developmental stages and subjected to DNA laddering analysis ( Yu et al, 2017 ).…”

Nitric oxide contributes to methane-induced osmotic stress tolerance in mung bean

“…Biosynthesis of NO is catalyzed by nitrate reductase (NR), a well-known route of reductive reactions, and nitric oxide synthesis (NOS)-like biochemical pathway [ 25 , 26 ]. Previously, there are more evidence showed that NO could modulate ROS generation, which is always accompanied by oxidative stress, to keep redox homeostasis and decrease oxidative damage [ 18 , 27 ]. Specific plant proteins involved in metabolism, stress responses, and redox homeostasis, have also been identified as possible targets for S -nitrosylation, one of NO-dependent post-translational modifications [ 28 , 29 ].…”

A point mutation in LTT1 enhances cold tolerance at the booting stage in rice

“…ROS are important signalling molecules necessary for multiple biological processes (Mittler, ) and play a key role in tapetal PCD (Yu et al, ). Failure to remove the excessively accumulated ROS in the tapetum would result in male sterility by causing precocious tapetal PCD (Hu et al, ; Luo et al, ; Xie et al, ).…”

“…The timely initiation of tapetal PCD during microspore development is found to be largely affected by dynamic changes of the endogenous level of reactive oxygen species (ROS; Hu et al, ; Ko et al, ; Xie, Wan, Li, & Zhang, ; Yu, Feng, Xie, Li, & Zhang, ), which are key signalling molecules involved in various biological processes and stress responses (Mittler, ). Relevant researches have unveiled that the cellular ROS level is very sensitive to temperature changes, and maintaining ROS homeostasis associates intimately with the adaptation to extreme temperature in rice (Baxter, Mittler, & Suzuki, ; Zhang et al, ).…”