Advances Towards How Meiotic Recombination Is Initiated: A Comparative View and Perspectives for Plant Meiosis Research.

Ju-Li Jing,Yan He,Ya-Zhong Wang,Ting Zhang

doi:10.3390/ijms20194718

Abstract

Meiosis is an essential cell-division process for ensuring genetic diversity across generations. Meiotic recombination ensures the accuracy of genetic interchange between homolous chromosomes and segregation of parental alleles. Programmed DNA double-strand breaks (DSBs), catalyzed by the evolutionarily conserved topoisomerase VIA (a subunit of the archaeal type II DNA topoisomerase)-like enzyme Spo11 and several other factors, is a distinctive feature of meiotic recombination initiation. The meiotic DSB formation and its regulatory mechanisms are similar among species, but certain aspects are distinct. In this review, we introduced the cumulative knowledge of the plant proteins crucial for meiotic DSB formation and technical advances in DSB detection. We also summarized the genome-wide DSB hotspot profiles for different model organisms. Moreover, we highlighted the classical views and recent advances in our knowledge of the regulatory mechanisms that ensure the fidelity of DSB formation, such as multifaceted kinase-mediated phosphorylation and the consequent high-dimensional changes in chromosome structure. We provided an overview of recent findings concerning DSB formation, distribution and regulation, all of which will help us to determine whether meiotic DSB formation is evolutionarily conserved or varies between plants and other organisms.

Highlights

In flowering plants, reproductive cells develop in the ‘sporophytic generation’ and differentiate into the gamete-forming ‘gametophytic generation’ [1,2]
The core molecular processes that generate double-strand breaks (DSBs) are largely conserved between plants and other species, the exact mechanisms involved vary among species
We introduced a generalized framework for the key players and regulatory pathways that produce DSBs and compare the conserved and non-conserved mechanisms of recombination initiation between plants and other species

Summary

Introduction

Reproductive cells develop in the ‘sporophytic generation’ and differentiate into the gamete-forming ‘gametophytic generation’ [1,2]. The participation of OsSPO11-1, OsSPO11-4 and OsMTOPVIB in DSB formation is conserved, as is their homologs in other species [83,84,85,86], the homologs of OsSDS and OsCRC1 in Arabidopsis, which are SDS and PCH2, respectively, are not required for DSB formation [87,88] These findings indicate that the DSB-forming machinery has substantially diverged between monocot and dicot plants. The rice P31comet, named OsBVF1 in an independent study, was unambiguously demonstrated to be required for DSB formation [90,91] Taken together, these results indicate that, except for Spo proteins, few of the other Spo accessory proteins are conserved at the sequence or functional level across the eukaryotic kingdoms

Defining Meiotic DSB Hotspots in Different Species

Control of Meiotic DSB Formation by Protein Phosphorylation

Concluding Remarks