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

^*Corresponding author for this work

Department of Life Sciences

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

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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
Article number	2563
Number of pages	13
Journal	Nature Communications
Volume	12
Issue number	1
Early online date	07 May 2021
DOIs	https://doi.org/10.1038/s41467-021-22920-8
Publication status	Published - 01 Dec 2021

Keywords

Avena/genetics
Disease Resistance/genetics
Edible Grain/genetics
Evolution, Molecular
High-Throughput Nucleotide Sequencing
In Situ Hybridization, Fluorescence
Metabolic Networks and Pathways/genetics
Multigene Family
RNA-Seq
Repetitive Sequences, Nucleic Acid
Saponins/biosynthesis
Synteny/genetics
Telomere/genetics
Tobacco/metabolism
Whole Genome Sequencing
Nicotiana/metabolism

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ArticleFinal published version, 3.7 MBLicence: CC BY
Supplementary informationData, 3.35 MBLicence: CC BY
Description of Additional Supplementary FilesData, 12.2 KBLicence: CC BY
Additional Supplementary FilesData, 92.7 KBLicence: CC BY
Source DataData, 765 KBLicence: CC BY

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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), Article 2563. https://doi.org/10.1038/s41467-021-22920-8

@article{065cfcf510164294ac0a8293e645e45a,

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.",

keywords = "Avena/genetics, Disease Resistance/genetics, Edible Grain/genetics, Evolution, Molecular, High-Throughput Nucleotide Sequencing, In Situ Hybridization, Fluorescence, Metabolic Networks and Pathways/genetics, Multigene Family, RNA-Seq, Repetitive Sequences, Nucleic Acid, Saponins/biosynthesis, Synteny/genetics, Telomere/genetics, Tobacco/metabolism, Whole Genome Sequencing, Nicotiana/metabolism",

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 = "Funding Information: We thank Zemin Ning (Sanger Institute) for assistance with genome assembly. Zde{\v n}ka Dubsk{\'a}, Romana {\v S}perkov{\'a} and Jitka Weiserov{\'a} for assistance with chromosome flow sorting, and Petr C{\'a}pal for PCR analysis of flow-sorted chromosomes with primers for the Sad1 gene. This research was supported by the Centre of Excellence for Plant and Microbial Sciences (CEPAMS), established between the John Innes Centre and the Chinese Academy of Sciences and funded by the UK Biotechnology and Biological Sciences Research Council (BBSRC), and the Chinese Academy of Sciences; International Partnership Program (IPP) of Chinese Academy of Sciences grant IPP/ 153D31KYSB20160074 and CAS grant XDPB0400; Biotechnology and Biological Sciences (BBSRC) grant BBSRC (BB/K005952/1); the joint Engineering and Physical Sciences Research Council/BBSRC-funded OpenPlant Synthetic Biology Research Centre grant BB/L014130/1 (M.S., A.O.); National Institutes of Health Genome to Natural Products Network award U101GM110699 (J.R., A.O.); John Innes Centre Innovation Fund grant IF2015BW22 (B.S., B.W., A.O). A.O.{\textquoteright}s programme is supported by the BBSRC Institute Strategic Programme Grant {\textquoteleft}Molecules from Nature – Products and Pathways{\textquoteright} (BBS/E/J/000PR9790) and the John Innes Foundation. G.P. is supported by a Royal Society Newton Fellowship, and R.C. by a BBSRC DTP award. B.H.{\textquoteright}s programme is supported by the National Natural Science Foundation of China Grant {\textquoteleft}Molecular Design for Future Crops{\textquoteright} (31788103). M.K., J.V. and J.D. were supported by the ERDF project {\textquoteleft}Plants as a tool for sustainable global development{\textquoteright} (No. CZ.02.1.01/0.0/0.0/ 16_019/0000827). Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = dec,

day = "1",

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

language = "English",

volume = "12",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Springer Nature",

number = "1",

}

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, 2563. https://doi.org/10.1038/s41467-021-22920-8

TY - JOUR

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 - Funding Information: We thank Zemin Ning (Sanger Institute) for assistance with genome assembly. Zdeňka Dubská, Romana Šperková and Jitka Weiserová for assistance with chromosome flow sorting, and Petr Cápal for PCR analysis of flow-sorted chromosomes with primers for the Sad1 gene. This research was supported by the Centre of Excellence for Plant and Microbial Sciences (CEPAMS), established between the John Innes Centre and the Chinese Academy of Sciences and funded by the UK Biotechnology and Biological Sciences Research Council (BBSRC), and the Chinese Academy of Sciences; International Partnership Program (IPP) of Chinese Academy of Sciences grant IPP/ 153D31KYSB20160074 and CAS grant XDPB0400; Biotechnology and Biological Sciences (BBSRC) grant BBSRC (BB/K005952/1); the joint Engineering and Physical Sciences Research Council/BBSRC-funded OpenPlant Synthetic Biology Research Centre grant BB/L014130/1 (M.S., A.O.); National Institutes of Health Genome to Natural Products Network award U101GM110699 (J.R., A.O.); John Innes Centre Innovation Fund grant IF2015BW22 (B.S., B.W., A.O). A.O.’s programme is supported by the BBSRC Institute Strategic Programme Grant ‘Molecules from Nature – Products and Pathways’ (BBS/E/J/000PR9790) and the John Innes Foundation. G.P. is supported by a Royal Society Newton Fellowship, and R.C. by a BBSRC DTP award. B.H.’s programme is supported by the National Natural Science Foundation of China Grant ‘Molecular Design for Future Crops’ (31788103). M.K., J.V. and J.D. were supported by the ERDF project ‘Plants as a tool for sustainable global development’ (No. CZ.02.1.01/0.0/0.0/ 16_019/0000827). Publisher Copyright: © 2021, The Author(s).

PY - 2021/12/1

Y1 - 2021/12/1

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.

KW - Avena/genetics

KW - Disease Resistance/genetics

KW - Edible Grain/genetics

KW - Evolution, Molecular

KW - High-Throughput Nucleotide Sequencing

KW - In Situ Hybridization, Fluorescence

KW - Metabolic Networks and Pathways/genetics

KW - Multigene Family

KW - RNA-Seq

KW - Repetitive Sequences, Nucleic Acid

KW - Saponins/biosynthesis

KW - Synteny/genetics

KW - Telomere/genetics

KW - Tobacco/metabolism

KW - Whole Genome Sequencing

KW - Nicotiana/metabolism

UR - http://www.scopus.com/inward/record.url?scp=85105527354&partnerID=8YFLogxK

U2 - 10.1038/s41467-021-22920-8

DO - 10.1038/s41467-021-22920-8

M3 - Article

C2 - 33963185

AN - SCOPUS:85105527354

SN - 2041-1723

VL - 12

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 2563

ER -

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

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