Mitochondrial Dysfunction Causes Oxidative Stress and Tapetal Apoptosis in Chemical Hybridization Reagent-Induced Male Sterility in Wheat

Abstract

Male sterility in plants has been strongly linked to mitochondrial dysfunction. Chemical hybridization agent (CHA)-induced male sterility is an important tool in crop heterosis. Therefore, it is important to better understand the relationship between mitochondria and CHA-induced male sterility in wheat. This study reports on the impairment of mitochondrial function duo to CHA-SQ-1, which occurs by decreasing cytochrome oxidase and adenosine triphosphate synthase protein levels and theirs activities, respiratory rate, and in turn results in the inhibition of the mitochondrial electron transport chain (ETC), excessive production of reactive oxygen species (ROS) and disruption of the alternative oxidase pathway. Subsequently, excessive ROS combined with MnSOD defects results in damage to the mitochondrial membrane, followed by ROS release into the cytoplasm. The microspores underwent severe oxidative stress during pollen development. Furthermore, chronic oxidative stress, together with the overexpression of type II metacaspase, triggered premature tapetal apoptosis, which resulted in pollen abortion. Accordingly, we propose a metabolic pathway for mitochondrial-mediated male sterility in wheat, which provides information on the molecular events underlying CHA-SQ-1-induced abortion of anthers and may serve as an additional guide to the practical application of hybrid breeding.

Tapetal-Delayed Programmed Cell Death (PCD) and Oxidative Stress-Induced Male Sterility of Aegilops uniaristata Cytoplasm in Wheat

“…Many studies suggested that the over-accumulation of ROS can also affect the expression of various genes by oxidative damage [ 42 , 43 ]. Moreover, previous studies on the mitochondrial genome have revealed some genes or open reading frames (ORFs) are often chimeric and co-transcribed with genes that encode the mitochondrial subunits of the respiratory enzymes related to ROS release and further indicated that mutation and recombination have a direct relationship with CMS [ 20 , 44 , 45 ]. In our study, we performed RT-PCR to determine the expression levels of the genes encoding important antioxidant enzymes.…”

The initial deficiency of protein processing and flavonoids biosynthesis were the main mechanisms for the male sterility induced by SX-1 in Brassica napus

“…TM resulted in BCAA starvation by anther-specific acetolactate synthase ( ALS ) inhibition and autophagic cell death in anthers [ 9 ]. The oxidative stress and overexpression of type II metacaspase in SQ-1 treated wheat would trigger premature tapetal apoptosis, and then result in pollen abortion [ 12 , 13 ]. Here, we found the new ALS inhibitor SX-1 can be used as an effective CHA to induce male sterility in B. napus .…”

“…In addition, CIMS doesn’t need prior selecting to match maintainer and restorer lines like CMS or remove the fertile plants from the female parents as half offspring of GMS are fertile [ 7 ]. Therefore, CHAs are getting more and more attention and have been widely applied, such as tribenuron-methyl (TM) [ 8 , 9 ], monosulphuron ester sodium (MES) [ 10 , 11 ] in B. napus and SQ-1 in Triticum aestivum [ 12 , 13 ]. In MES induced male sterility, genes involved in cellular transport, lipid and carbohydrate metabolism were differentially expressed [ 11 ].…”

“…While the mutation of ALS with a substitution of proline with leucine or serine at position 197 will gain the resistance of TM and exhibit normal male fertility [ 8 ]. In SQ-1 treated wheat, premature tapetum degraded in advance and the defective in carbohydrate metabolism and oxidase pathway were the reason for the occurrence of pollen sterile [ 12 , 13 ].…”

Cyclin-Dependent Kinase Inhibitor Gene TaICK1 acts as a Potential Contributor to Wheat Male Sterility induced by a Chemical Hybridizing Agent

“…Nevertheless, the molecular mechanism underlying SQ-1-induced wheat male sterility remains relatively unknown, representing an impediment to the application of SQ-1-induced wheat male sterility. Previous research has indicated that pollen abortion may be associated with impaired energy metabolism after spraying of SQ-1 [17][18][19][20][21][22][23]. For example, SQ-1-induced sterility lines showed lower expression levels of the PDH-E1α gene, which is essential for regulation of the tricarboxylic acid (TAC) cycle [24].…”