Multiple genes recruited from hormone pathways partition maize diterpenoid defences

doi:10.1038/s41477-019-0509-6

. 2019 Oct;5(10):1043-1056.

doi: 10.1038/s41477-019-0509-6. Epub 2019 Sep 16.

Multiple genes recruited from hormone pathways partition maize diterpenoid defences

Yezhang Ding¹, Katherine M Murphy², Elly Poretsky¹, Sibongile Mafu², Bing Yang³, Si Nian Char³, Shawn A Christensen⁴, Evan Saldivar¹, Mengxi Wu¹, Qiang Wang⁵, Lexiang Ji⁶, Robert J Schmitz⁷, Karl A Kremling⁸, Edward S Buckler^{8

9}, Zhouxin Shen¹, Steven P Briggs¹, Jörg Bohlmann¹⁰, Andrew Sher¹, Gabriel Castro-Falcon¹¹, Chambers C Hughes¹¹, Alisa Huffaker¹, Philipp Zerbe², Eric A Schmelz¹²

Affiliations

¹ Section of Cell and Developmental Biology, University of California San Diego, La Jolla, CA, USA.
² Department of Plant Biology, University of California Davis, Davis, CA, USA.
³ Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA, USA.
⁴ Chemistry Research Unit, Center for Medical, Agricultural, and Veterinary Entomology, US Department of Agriculture-Agricultural Research Service, Gainesville, FL, USA.
⁵ Institute of Ecological Agriculture, Sichuan Agricultural University, Chengdu, China.
⁶ Institute of Bioinformatics, University of Georgia, Athens, GA, USA.
⁷ Department of Genetics, University of Georgia, Athens, GA, USA.
⁸ Department of Plant Breeding and Genetics, Cornell University, Ithaca, NY, USA.
⁹ Robert W. Holley Center for Agriculture and Health, US Department of Agriculture-Agricultural Research Service, Ithaca, NY, USA.
¹⁰ Michael Smith Laboratories, University of British Columbia, Vancouver, British Columbia, Canada.
¹¹ Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA, USA.
¹² Section of Cell and Developmental Biology, University of California San Diego, La Jolla, CA, USA. eschmelz@ucsd.edu.

PMID: 31527844
DOI: 10.1038/s41477-019-0509-6

Multiple genes recruited from hormone pathways partition maize diterpenoid defences

Yezhang Ding et al. Nat Plants. 2019 Oct.

. 2019 Oct;5(10):1043-1056.

doi: 10.1038/s41477-019-0509-6. Epub 2019 Sep 16.

Authors

Affiliations

¹ Section of Cell and Developmental Biology, University of California San Diego, La Jolla, CA, USA.
² Department of Plant Biology, University of California Davis, Davis, CA, USA.
³ Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA, USA.
⁴ Chemistry Research Unit, Center for Medical, Agricultural, and Veterinary Entomology, US Department of Agriculture-Agricultural Research Service, Gainesville, FL, USA.
⁵ Institute of Ecological Agriculture, Sichuan Agricultural University, Chengdu, China.
⁶ Institute of Bioinformatics, University of Georgia, Athens, GA, USA.
⁷ Department of Genetics, University of Georgia, Athens, GA, USA.
⁸ Department of Plant Breeding and Genetics, Cornell University, Ithaca, NY, USA.
⁹ Robert W. Holley Center for Agriculture and Health, US Department of Agriculture-Agricultural Research Service, Ithaca, NY, USA.
¹⁰ Michael Smith Laboratories, University of British Columbia, Vancouver, British Columbia, Canada.
¹¹ Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA, USA.
¹² Section of Cell and Developmental Biology, University of California San Diego, La Jolla, CA, USA. eschmelz@ucsd.edu.

PMID: 31527844
DOI: 10.1038/s41477-019-0509-6

Abstract

Duplication and divergence of primary pathway genes underlie the evolution of plant specialized metabolism; however, mechanisms partitioning parallel hormone and defence pathways are often speculative. For example, the primary pathway intermediate ent-kaurene is essential for gibberellin biosynthesis and is also a proposed precursor for maize antibiotics. By integrating transcriptional coregulation patterns, genome-wide association studies, combinatorial enzyme assays, proteomics and targeted mutant analyses, we show that maize kauralexin biosynthesis proceeds via the positional isomer ent-isokaurene formed by a diterpene synthase pair recruited from gibberellin metabolism. The oxygenation and subsequent desaturation of ent-isokaurene by three promiscuous cytochrome P450s and a new steroid 5α reductase indirectly yields predominant ent-kaurene-associated antibiotics required for Fusarium stalk rot resistance. The divergence and differential expression of pathway branches derived from multiple duplicated hormone-metabolic genes minimizes dysregulation of primary metabolism via the circuitous biosynthesis of ent-kaurene-related antibiotics without the production of growth hormone precursors during defence.

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References

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1. Lopez-Nieves, S. et al. Relaxation of tyrosine pathway regulation underlies the evolution of betalain pigmentation in Caryophyllales. New Phytol. 217, 896–908 (2018). - PubMed

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[1] Dixon, R. A. Natural products and plant disease resistance. Nature 411, 843–847 (2001). - PubMed

[2] Dixon, R. A. Natural products and plant disease resistance. Nature 411, 843–847 (2001). - PubMed

[3] Gershenzon, J. & Dudareva, N. The function of terpene natural products in the natural world. Nat. Chem. Biol. 3, 408–414 (2007). - PubMed

[4] Gershenzon, J. & Dudareva, N. The function of terpene natural products in the natural world. Nat. Chem. Biol. 3, 408–414 (2007). - PubMed

[5] Pichersky, E. & Lewinsohn, E. Convergent evolution in plant specialized metabolism. Ann. Rev. Plant Biol. 62, 549–566 (2011).

[6] Pichersky, E. & Lewinsohn, E. Convergent evolution in plant specialized metabolism. Ann. Rev. Plant Biol. 62, 549–566 (2011).

[7] Turlings, T. C. J. & Erb, M. Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu. Rev. Entomol. 63, 433–452 (2018). - PubMed

[8] Turlings, T. C. J. & Erb, M. Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu. Rev. Entomol. 63, 433–452 (2018). - PubMed

[9] Lopez-Nieves, S. et al. Relaxation of tyrosine pathway regulation underlies the evolution of betalain pigmentation in Caryophyllales. New Phytol. 217, 896–908 (2018). - PubMed

[10] Lopez-Nieves, S. et al. Relaxation of tyrosine pathway regulation underlies the evolution of betalain pigmentation in Caryophyllales. New Phytol. 217, 896–908 (2018). - PubMed

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Multiple genes recruited from hormone pathways partition maize diterpenoid defences

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Multiple genes recruited from hormone pathways partition maize diterpenoid defences

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