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; Anne Osbourn

doi:10.1038/s41467-021-22920-8

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. StephensonLei 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, Anne Osbourn

Research output: Contribution to journal › Article › peer-review

53 Scopus citations

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.

Original language	English (US)
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-22920-8
State	Published - Dec 1 2021
Externally published	Yes

Bibliographical note

Generated from Scopus record by KAUST IRTS on 2023-02-20

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology
General Chemistry
General Physics and Astronomy

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Li, Y., Leveau, A., Zhao, Q., Feng, Q., Lu, H., Miao, J., Xue, Z., Martin, A. C., Wegel, E., Wang, J., Orme, A., Rey, M. D., Karafiátová, M., Vrána, J., Steuernagel, B., Joynson, R., Owen, C., Reed, J., Louveau, T., ... Osbourn, A. (2021). Subtelomeric assembly of a multi-gene pathway for antimicrobial defense compounds in cereals. Nature Communications, 12(1). https://doi.org/10.1038/s41467-021-22920-8

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title = "Subtelomeric assembly of a multi-gene pathway for antimicrobial defense compounds in cereals",

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 {\textquoteleft}self-poisoning{\textquoteright} 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.",

author = "Yan Li and Aymeric Leveau and Qiang Zhao and Qi Feng and Hengyun Lu and Jiashun Miao and Zheyong Xue and Martin, {Azahara C.} and Eva Wegel and Jing Wang and Anastasia Orme and Rey, {Maria Dolores} and Miroslava Karafi{\'a}tov{\'a} and Jan Vr{\'a}na and Burkhard Steuernagel and Ryan Joynson and Charlotte Owen and James Reed and Thomas Louveau and Stephenson, {Michael J.} and Lei Zhang and Xuehui Huang and Tao Huang and Danling Fan and Congcong Zhou and Qilin Tian and Wenjun Li and Yiqi Lu and Jiaying Chen and Yan Zhao and Ying Lu and Chuanrang Zhu and Zhenhua Liu and Guy Polturak and Rebecca Casson and Lionel Hill and Graham Moore and Rachel Melton and Neil Hall and Wulff, {Brande B.H.} and Jaroslav Dole{\v z}el and Tim Langdon and Bin Han and Anne Osbourn",

note = "Generated from Scopus record by KAUST IRTS on 2023-02-20",

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doi = "10.1038/s41467-021-22920-8",

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Li, Y, Leveau, A, Zhao, Q, Feng, Q, Lu, H, Miao, J, Xue, Z, Martin, AC, Wegel, E, Wang, J, Orme, A, Rey, MD, Karafiátová, M, Vrána, J, Steuernagel, B, Joynson, R, Owen, C, Reed, J, Louveau, T, Stephenson, MJ, Zhang, L, Huang, X, Huang, T, Fan, D, Zhou, C, Tian, Q, Li, W, Lu, Y, Chen, J, Zhao, Y, Lu, Y, Zhu, C, Liu, Z, Polturak, G, Casson, R, Hill, L, Moore, G, Melton, R, Hall, N, Wulff, BBH, Doležel, J, Langdon, T, Han, B & Osbourn, A 2021, 'Subtelomeric assembly of a multi-gene pathway for antimicrobial defense compounds in cereals', Nature Communications, vol. 12, no. 1. https://doi.org/10.1038/s41467-021-22920-8

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T1 - Subtelomeric assembly of a multi-gene pathway for antimicrobial defense compounds in cereals

AU - Li, Yan

AU - Leveau, Aymeric

AU - Zhao, Qiang

AU - Feng, Qi

AU - Lu, Hengyun

AU - Miao, Jiashun

AU - Xue, Zheyong

AU - Martin, Azahara C.

AU - Wegel, Eva

AU - Wang, Jing

AU - Orme, Anastasia

AU - Rey, Maria Dolores

AU - Karafiátová, Miroslava

AU - Vrána, Jan

AU - Steuernagel, Burkhard

AU - Joynson, Ryan

AU - Owen, Charlotte

AU - Reed, James

AU - Louveau, Thomas

AU - Stephenson, Michael J.

AU - Zhang, Lei

AU - Huang, Xuehui

AU - Huang, Tao

AU - Fan, Danling

AU - Zhou, Congcong

AU - Tian, Qilin

AU - Li, Wenjun

AU - Lu, Yiqi

AU - Chen, Jiaying

AU - Zhao, Yan

AU - Lu, Ying

AU - Zhu, Chuanrang

AU - Liu, Zhenhua

AU - Polturak, Guy

AU - Casson, Rebecca

AU - Hill, Lionel

AU - Moore, Graham

AU - Melton, Rachel

AU - Hall, Neil

AU - Wulff, Brande B.H.

AU - Doležel, Jaroslav

AU - Langdon, Tim

AU - Han, Bin

AU - Osbourn, Anne

N1 - Generated from Scopus record by KAUST IRTS on 2023-02-20

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N2 - 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.

AB - 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.

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U2 - 10.1038/s41467-021-22920-8

DO - 10.1038/s41467-021-22920-8

M3 - Article

SN - 2041-1723

VL - 12

JO - Nature Communications

JF - Nature Communications

IS - 1

ER -

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

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ASJC Scopus subject areas

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