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

Yan Li, Aymeric Leveau, Qiang Zhao, Qi Feng, Hengyun Lu, Jiashun Miao, Zheyong Xue, Azahara C. Martin, Eva Wegel, Jing Wang, Anastasia Orme, Maria-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 Lu, Chuanrang Zhu, Zhenhua Liu, Guy Polturak, Rebecca Casson, Lionel Hill, Graham Moore, Rachel Melton, Neil Hall, Brande B. H. Wulff, Jaroslav Doležel, Tim Langdon, Bin Han () and Anne Osbourn ()
Additional contact information
Yan Li: Chinese Academy of Sciences (CAS)
Aymeric Leveau: John Innes Centre, Norwich Research Park
Qiang Zhao: Chinese Academy of Sciences (CAS)
Qi Feng: Chinese Academy of Sciences (CAS)
Hengyun Lu: Chinese Academy of Sciences (CAS)
Jiashun Miao: Chinese Academy of Sciences (CAS)
Zheyong Xue: John Innes Centre, Norwich Research Park
Azahara C. Martin: John Innes Centre, Norwich Research Park
Eva Wegel: John Innes Centre, Norwich Research Park
Jing Wang: John Innes Centre, Norwich Research Park
Anastasia Orme: John Innes Centre, Norwich Research Park
Maria-Dolores Rey: John Innes Centre, Norwich Research Park
Miroslava Karafiátová: Centre of the Region Haná for Biotechnological and Agricultural Research
Jan Vrána: Centre of the Region Haná for Biotechnological and Agricultural Research
Burkhard Steuernagel: John Innes Centre, Norwich Research Park
Ryan Joynson: Earlham Institute, Norwich Research Park
Charlotte Owen: John Innes Centre, Norwich Research Park
James Reed: John Innes Centre, Norwich Research Park
Thomas Louveau: John Innes Centre, Norwich Research Park
Michael J. Stephenson: John Innes Centre, Norwich Research Park
Lei Zhang: Chinese Academy of Sciences (CAS)
Xuehui Huang: Chinese Academy of Sciences (CAS)
Tao Huang: Chinese Academy of Sciences (CAS)
Danling Fan: Chinese Academy of Sciences (CAS)
Congcong Zhou: Chinese Academy of Sciences (CAS)
Qilin Tian: Chinese Academy of Sciences (CAS)
Wenjun Li: Chinese Academy of Sciences (CAS)
Yiqi Lu: Chinese Academy of Sciences (CAS)
Jiaying Chen: Chinese Academy of Sciences (CAS)
Yan Zhao: Chinese Academy of Sciences (CAS)
Ying Lu: Chinese Academy of Sciences (CAS)
Chuanrang Zhu: Chinese Academy of Sciences (CAS)
Zhenhua Liu: Shanghai Jiao Tong University
Guy Polturak: John Innes Centre, Norwich Research Park
Rebecca Casson: John Innes Centre, Norwich Research Park
Lionel Hill: John Innes Centre, Norwich Research Park
Graham Moore: John Innes Centre, Norwich Research Park
Rachel Melton: John Innes Centre, Norwich Research Park
Neil Hall: Earlham Institute, Norwich Research Park
Brande B. H. Wulff: John Innes Centre, Norwich Research Park
Jaroslav Doležel: Centre of the Region Haná for Biotechnological and Agricultural Research
Tim Langdon: Aberystwyth University, Gogerddan
Bin Han: Chinese Academy of Sciences (CAS)
Anne Osbourn: John Innes Centre, Norwich Research Park

Nature Communications, 2021, vol. 12, issue 1, 1-13

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-22920-8

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