Genomic view of heavy-ion-induced deletions associated with distribution of essential genes in Arabidopsis thaliana

Front Plant Sci. 2024 Apr 17:15:1352564. doi: 10.3389/fpls.2024.1352564. eCollection 2024.

Abstract

Heavy-ion beam, a type of ionizing radiation, has been applied to plant breeding as a powerful mutagen and is a promising tool to induce large deletions and chromosomal rearrangements. The effectiveness of heavy-ion irradiation can be explained by linear energy transfer (LET; keV µm-1). Heavy-ion beams with different LET values induce different types and sizes of mutations. It has been suggested that deletion size increases with increasing LET value, and complex chromosomal rearrangements are induced in higher LET radiations. In this study, we mapped heavy-ion beam-induced deletions detected in Arabidopsis mutants to its genome. We revealed that deletion sizes were similar between different LETs (100 to 290 keV μm-1), that their upper limit was affected by the distribution of essential genes, and that the detected chromosomal rearrangements avoid disrupting the essential genes. We also focused on tandemly arrayed genes (TAGs), where two or more homologous genes are adjacent to one another in the genome. Our results suggested that 100 keV µm-1 of LET is enough to disrupt TAGs and that the distribution of essential genes strongly affects the heritability of mutations overlapping them. Our results provide a genomic view of large deletion inductions in the Arabidopsis genome.

Keywords: Arabidopsis thaliana; essential gene; heavy-ion beam; linear energy transfer; mutagenesis; tandemly arrayed gene.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. TA was supported by Cross-ministerial Strategic Innovation Promotion Program (SIP), ‘Technologies for creating next-generation agriculture, forestry and fisheries’ (funding agency Bio-oriented Technology Research Advancement Institution, NARO) and was also supported by the Joint Research Program between RIKEN and Fukui Prefecture. Funding to support this research was provided to YK (Grant Numbers JP20H03297, JP20K21449, JP21KK0128, and JP22H05071) and KI (Grant Number JP19K06622) by JSPS KAKENHI.