Subtelomeric assembly of a multi-gene pathway for antimicrobial defense compounds in cereals

Hengyun Lu,Wenjun Li,Qi Feng,Guy Polturak,Thomas Louveau,Lei Zhang,Yan Zhao,Ying Lu,Tim Langdon,Ryan Joynson,Bin Han,Graham Moore,Rachel E Melton ,Chuanrang Zhu,James Reed,Qiang Zhao,Brande B H Wulff,Danling Fan,Xuehui Huang,Charlie Owen ,Yan Li,Anastasia Orme,Lionel Hill,Michael J Stephenson,Jiaying Chen,Rebecca Casson,Zhenhua Liu,Aymeric Leveau,Jiashun Miao,Yiqi Lu,Neil Hall,María Rey ,Eva Wegel,Zheyong Xue,Jan Vrána,Qifeng Tian ,Burkhard Steuernagel,Tao Huang,Anne Osbourn,Azahara C Martín ,Miroslava Karafiátová,Jaroslav Doležel,Congcong Zhou,Jing Wang

doi:10.1038/s41467-021-22920-8

Abstract

Non-random gene organization in eukaryotes plays a significant role in genome evolution. Here, we investigate the origin of a biosynthetic gene cluster for production of defence compounds in oat—the avenacin cluster. We elucidate the structure and organisation of this 12-gene cluster, characterise the last two missing pathway steps, and reconstitute the entire pathway in tobacco by transient expression. We show that the cluster has formed de novo since the divergence of oats in a subtelomeric region of the genome that lacks homology with other grasses, and that gene order is approximately colinear with the biosynthetic pathway. We speculate that the positioning of the late pathway genes furthest away from the telomere may mitigate against a ‘self-poisoning’ scenario in which toxic intermediates accumulate as a result of telomeric gene deletions. Our investigations reveal a striking example of adaptive evolution underpinned by remarkable genome plasticity.

Highlights

Non-random gene organization in eukaryotes plays a significant role in genome evolution
To elucidate the complete avenacin cluster and investigate its origin we first sequenced the genome of A. strigosa accession S75 (2n = 14), the accession used in our original forward mutant screen for identification of avenacin pathway mutants[2]
In summary, our genomics-driven approach has shed light on the organisation and evolution of a complex biosynthetic gene cluster required for disease resistance in oat

Summary

Introduction

Non-random gene organization in eukaryotes plays a significant role in genome evolution. We show that the cluster has formed de novo since the divergence of oats in a subtelomeric region of the genome that lacks homology with other grasses, and that gene order is approximately colinear with the biosynthetic pathway. A intriguing question concerns the mechanisms by which these clusters of non-homologous yet functionally related genes arise, presumably in response to a particular set of selective pressures Understanding how these clusters form and what the significance of clustering is will be crucial in understanding the relationship between genome organisation and the evolution of complex adaptive traits in eukaryotes. We employ a genomics-driven approach to investigate the nature and origin of the avenacin cluster in diploid oat and show that this 12-gene cluster has formed de novo in a subtelomeric region of chromosome 1 that lacks homology with other grasses. Our study sheds light on the mechanisms shaping genome architecture and adaptive evolution in plants

Methods

Results

Conclusion