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Matrilineal empowers wheat pollen with haploid induction potency via triggering post-mitosis ROS activity.

Reactive Oxygen Species (ROS) plays important roles during anther and pollen development. DNA damages may cause chromosome fragmentation that is considered to underlie chromosome elimination for haploid induction by matrilineal pollen, a key step in MATRILINEAL-based double haploid breeding technology. But when and how DNA damages occur is unknown. We performed comparative studies of wheat pollens from the wild type and the CRISPR/Cas9 edited matrilineal mutant (mMTL). Chemical assays detected a second wave of ROS in mMTL pollen at three-nuclei-stage and onwards, along with reduced antioxidant enzyme activities. RNA-seq analysis revealed disturbed expression of genes for fatty acid biosynthesis and ROS homoeostasis. GC-MS measurement identified abnormal fatty acid metabolism which may contribute to defective mMTL pollen walls as observed by electron microscopy, consistent with the function of MTL as a phospholipase. Moreover, DNA damages were identified by TUNEL and quantified by Comet assays. Velocity patterns showed that ROS increments preceded that of DNA damage over the course of pollen maturation. Our work hypothesizes that mMTL-triggered later-stage specific ROS causes DNA damage which may contribute to chromosome elimination during haploid induction. The findings may provide additional niches to accelerate double haploid-based plant breeding.