In planta variation of volatile biosynthesis: an alternative biosynthetic route to the formation of the pathogen-induced volatile homoterpene DMNT via triterpene degradation in Arabidopsis roots.
Plant-derived volatile compounds such as terpenes exhibit substantial structural variation and serve multiple ecological functions. Despite their structural diversity, volatile terpenes are generally produced from a small number of core 5- to 20-carbon intermediates. Here, we present unexpected plasticity in volatile terpene biosynthesis by showing that irregular homo/norterpenes can arise from different biosynthetic routes in a tissue specific manner. While Arabidopsis thaliana and other angiosperms are known to produce the homoterpene (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) or its C16-analog (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene by the breakdown of sesquiterpene and diterpene tertiary alcohols in aboveground tissues, we demonstrate that Arabidopsis roots biosynthesize DMNT by the degradation of the C30 triterpene diol, arabidiol. The reaction is catalyzed by the Brassicaceae-specific cytochrome P450 monooxygenase CYP705A1 and is transiently induced in a jasmonate-dependent manner by infection with the root-rot pathogen Pythium irregulare. CYP705A1 clusters with the arabidiol synthase gene ABDS, and both genes are coexpressed constitutively in the root stele and meristematic tissue. We further provide in vitro and in vivo evidence for the role of the DMNT biosynthetic pathway in resistance against P. irregulare. Our results show biosynthetic plasticity in DMNT biosynthesis in land plants via the assembly of triterpene gene clusters and present biochemical and genetic evidence for volatile compound formation via triterpene degradation in plants.
Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia 24061.
Reza
http://orcid.org/0000-0003-1621-8496
R
Sohrabi
Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia 24061.
Jung-Hyun
JH
Huh
Department of Biochemistry, Virginia Tech, Blacksburg, Virginia 24061.
Somayesadat
S
Badieyan
Department of Chemistry, Virginia Tech, Blacksburg, Virginia 24061.
Liva Harinantenaina
LH
Rakotondraibe
Department of Plant Science, University of California, Davis, California 95616.
Daniel J
DJ
Kliebenstein
Department of Biochemistry, Virginia Tech, Blacksburg, Virginia 24061.
Pablo
P
Sobrado
Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia 24061 tholl@vt.edu.
Dorothea
http://orcid.org/0000-0003-2636-6345
D
Tholl
D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism* / Q000382:microbiology*; D053898:Biosynthetic Pathways; D002849:Chromatography, Gas; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D013058:Mass Spectrometry; D062105:Molecular Docking Simulation; D009928:Organ Specificity; D018517:Plant Roots / Q000235:genetics / Q000378:metabolism* / Q000382:microbiology; D011775:Pythium / Q000254:growth & development / Q000502:physiology; D012441:Saccharomyces cerevisiae / Q000378:metabolism; D013379:Substrate Specificity; D013729:Terpenes / Q000378:metabolism*; D014315:Triterpenes / Q000737:chemistry / Q000378:metabolism*; D055549:Volatile Organic Compounds / Q000378:metabolism*
C411254:4,8-dimethyl-1,3,7-nonatriene; D013729:Terpenes; D014315:Triterpenes; D055549:Volatile Organic Compounds; C521218:arabidiol