Subtelomeric assembly of a multi-gene pathway for antimicrobial defense compounds in cereals
Yán Li, Aymeric Leveau, Qiang Zhao, Qi Feng, Hengyun Lu, Jiashun Miao, Zheyong Xue, Azahara C. Martín, Eva Wegel, Jing Wang, Anastasia Orme, María-Dolores Rey, Miroslava Karafiátová, Jan Vrána, Burkhard Steuernagel, Ryan Joynson, Charlotte Owen, James Reed, Thomas Louveau, Michael J. Stephenson, Lei Zhang, Xuehui Huang, Tao Huang, Danling Fan, Congcong Zhou, Qilin Tian, Wenjun Li, Yiqi Lu, Jiaying Chen, Yan Zhao, Ying Lü, Chuanrang Zhu, Zhenhua Liu, Guy Polturak, Rebecca Casson, Lionel Hill, Graham Moore, Rachel E. Melton, Neil Hall, Brande B. H. Wulff, Jaroslav Doležel, Tim Langdon, Bin Han, Anne Osbourn
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.