The FATTY ACID DESATURASE2 Family in Tomato Contributes to Primary Metabolism and Stress Responses1[OPEN]

A gene family that is required for synthesis of polyunsaturated fatty acids also contributes to aphid resistance in tomato. The conversion of oleic acid (C18:1) to linoleic acid (C18:2) in the endoplasmic reticulum is critical to the accumulation of polyunsaturated fatty acids in seeds and other tis...

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Published in:Plant physiology (Bethesda) Vol. 182; no. 2; pp. 1083 - 1099
Main Authors: Lee, Min Woo, Padilla, Carmen S., Gupta, Chirag, Galla, Aravind, Pereira, Andy, Li, Jiamei, Goggin, Fiona L.
Format: Journal Article
Language:English
Published: American Society of Plant Biologists 25-11-2019
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Abstract A gene family that is required for synthesis of polyunsaturated fatty acids also contributes to aphid resistance in tomato. The conversion of oleic acid (C18:1) to linoleic acid (C18:2) in the endoplasmic reticulum is critical to the accumulation of polyunsaturated fatty acids in seeds and other tissues, and this reaction is catalyzed by a Δ12-desaturase, FATTY ACID DESATURASE2 (FAD2). Here, we report that the tomato ( Solanum lycopersicum ) genome harbors two genes, SlFAD2-1 and SlFAD2-2 , which encode proteins with in vitro Δ12-desaturase activity. In addition, tomato has seven divergent FAD2 members that lack Δ12-desaturase activity and differ from canonical FAD2 enzymes at multiple amino acid positions important to enzyme function. Whereas SlFAD2-1 and SlFAD2-2 are downregulated by biotic stress, the majority of divergent FAD2 genes in tomato are upregulated by one or more stresses. In particular, SlFAD2-7 is induced by the potato aphid ( Macrosiphum euphorbiae ) and has elevated constitutive expression levels in suppressor of prosystemin-mediated responses2 ( spr2 ), a tomato mutant with enhanced aphid resistance and altered fatty acid profiles. Virus-induced gene silencing of SlFAD2-7 in spr2 results in significant increases in aphid population growth, indicating that a divergent FAD2 gene contributes to aphid resistance in this genotype. Thus, the FAD2 gene family in tomato is important both to primary fatty acid metabolism and to responses to biotic stress.
AbstractList A gene family that is required for synthesis of polyunsaturated fatty acids also contributes to aphid resistance in tomato. The conversion of oleic acid (C18:1) to linoleic acid (C18:2) in the endoplasmic reticulum is critical to the accumulation of polyunsaturated fatty acids in seeds and other tissues, and this reaction is catalyzed by a Δ12-desaturase, FATTY ACID DESATURASE2 (FAD2). Here, we report that the tomato ( Solanum lycopersicum ) genome harbors two genes, SlFAD2-1 and SlFAD2-2 , which encode proteins with in vitro Δ12-desaturase activity. In addition, tomato has seven divergent FAD2 members that lack Δ12-desaturase activity and differ from canonical FAD2 enzymes at multiple amino acid positions important to enzyme function. Whereas SlFAD2-1 and SlFAD2-2 are downregulated by biotic stress, the majority of divergent FAD2 genes in tomato are upregulated by one or more stresses. In particular, SlFAD2-7 is induced by the potato aphid ( Macrosiphum euphorbiae ) and has elevated constitutive expression levels in suppressor of prosystemin-mediated responses2 ( spr2 ), a tomato mutant with enhanced aphid resistance and altered fatty acid profiles. Virus-induced gene silencing of SlFAD2-7 in spr2 results in significant increases in aphid population growth, indicating that a divergent FAD2 gene contributes to aphid resistance in this genotype. Thus, the FAD2 gene family in tomato is important both to primary fatty acid metabolism and to responses to biotic stress.
Author Gupta, Chirag
Pereira, Andy
Galla, Aravind
Li, Jiamei
Goggin, Fiona L.
Lee, Min Woo
Padilla, Carmen S.
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  givenname: Min Woo
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  organization: Department of Entomology and Plant Pathology, University of Arkansas, Fayetteville, Arkansas 72701
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  givenname: Carmen S.
  surname: Padilla
  fullname: Padilla, Carmen S.
  organization: Department of Entomology and Plant Pathology, University of Arkansas, Fayetteville, Arkansas 72701
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  organization: Department of Entomology and Plant Pathology, University of Arkansas, Fayetteville, Arkansas 72701
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  givenname: Andy
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  organization: Department of Crop, Soil, and Environmental Sciences, University of Arkansas, Fayetteville, Arkansas 72701
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  givenname: Jiamei
  surname: Li
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  organization: Department of Entomology and Plant Pathology, University of Arkansas, Fayetteville, Arkansas 72701
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  givenname: Fiona L.
  surname: Goggin
  fullname: Goggin, Fiona L.
  email: fgoggin@uark.edu
  organization: Department of Entomology and Plant Pathology, University of Arkansas, Fayetteville, Arkansas 72701
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Copyright 2020 American Society of Plant Biologists. All Rights Reserved. 2020
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Notes The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Fiona L. Goggin (fgoggin@uark.edu).
www.plantphysiol.org/cgi/doi/10.1104/pp.19.00487
Present address: U.S. Department of Agriculture, Agricultural Research Service–Cropping Systems and Water Quality Research Unit, 1680 Madison Ave., Wooster, OH 44691.
Present address: Texas A&M AgriLife Research and Extension Center, 2415 Business 83, Weslaco, TX 78596.
Senior author.
M.W.L. performed most of the experiments; C.S.P. and A.G. assisted with gene expression analysis; C.G. conducted bioinformatics analyses with supervision from A.P.; J.L. assisted with gas chromatography-mass spectrometry; F.L.G. conceived and supervised the project, assisted with statistical analyses, and completed the final manuscript with input from all authors.
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Title The FATTY ACID DESATURASE2 Family in Tomato Contributes to Primary Metabolism and Stress Responses1[OPEN]
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