TY - JOUR
T1 - Selinene volatiles are essential precursors for maize defense promoting fungal pathogen resistance
AU - Ding, Yezhang
AU - Huffaker, Alisa
AU - Köllner, Tobias G.
AU - Weckwerth, Philipp
AU - Robert, Christelle A.M.
AU - Spencer, Joseph L.
AU - Lipka, Alexander E.
AU - Schmelz, Eric A.
N1 - 1E.A.S. and A.H. gratefully acknowledge support by startup funds through the University of California San Diego, the DOE Joint Genome Institute Community Science Program (grant no. WIP 2568), and partial support for this work through a NSF-IOS Competitive Award (grant no. 1139329). With the support of Y. Yoshikuni, this research, or a portion thereof, was performed under the JGI-EMSL Collaborative Science Initiative and used resources at the DOE Joint Genome Institute and the Environmental Molecular Sciences Laboratory, which are DOE Office of Science user facilities. Both facilities are sponsored by the Office of Biological and Environmental Research and operated under contract numbers DE-AC02-05CH11231 (JGI) and DE-AC05-76RL01830 (EMSL). 2 Address correspondence to [email protected].
PY - 2017/11
Y1 - 2017/11
N2 - To ensure food security, maize (Zea mays) is a model crop for understanding useful traits underlying stress resistance. In contrast to foliar biochemicals, root defenses limiting the spread of disease remain poorly described. To better understand belowground defenses in the field, we performed root metabolomic profiling and uncovered unexpectedly high levels of the sesquiterpene volatile β-selinene and the corresponding nonvolatile antibiotic derivative β-costic acid. The application of metabolite-based quantitative trait locus mapping using biparental populations, genome-wide association studies, and nearisogenic lines enabled the identification of terpene synthase21 (ZmTps21) on chromosome 9 as a β-costic acid pathway candidate gene. Numerous closely examined b-costic acid-deficient inbred lines were found to harbor Zmtps21 pseudogenes lacking conserved motifs required for farnesyl diphosphate cyclase activity. For biochemical validation, a full-length ZmTps21 was cloned, heterologously expressed in Escherichia coli, and demonstrated to cyclize farnesyl diphosphate, yielding β-selinene as the dominant product. Consistent with microbial defense pathways, ZmTps21 transcripts strongly accumulate following fungal elicitation. Challenged field roots containing functional ZmTps21 alleles displayed b-costic acid levels over 100 µg g-1 fresh weight, greatly exceeding in vitro concentrations required to inhibit the growth of five different fungal pathogens and rootworm larvae (Diabrotica balteata). In vivo disease resistance assays, using ZmTps21 and Zmtps21 near-isogenic lines, further support the endogenous antifungal role of selinene-derived metabolites. Involved in the biosynthesis of nonvolatile antibiotics, ZmTps21 exists as a useful gene for germplasm improvement programs targeting optimized biotic stress resistance.
AB - To ensure food security, maize (Zea mays) is a model crop for understanding useful traits underlying stress resistance. In contrast to foliar biochemicals, root defenses limiting the spread of disease remain poorly described. To better understand belowground defenses in the field, we performed root metabolomic profiling and uncovered unexpectedly high levels of the sesquiterpene volatile β-selinene and the corresponding nonvolatile antibiotic derivative β-costic acid. The application of metabolite-based quantitative trait locus mapping using biparental populations, genome-wide association studies, and nearisogenic lines enabled the identification of terpene synthase21 (ZmTps21) on chromosome 9 as a β-costic acid pathway candidate gene. Numerous closely examined b-costic acid-deficient inbred lines were found to harbor Zmtps21 pseudogenes lacking conserved motifs required for farnesyl diphosphate cyclase activity. For biochemical validation, a full-length ZmTps21 was cloned, heterologously expressed in Escherichia coli, and demonstrated to cyclize farnesyl diphosphate, yielding β-selinene as the dominant product. Consistent with microbial defense pathways, ZmTps21 transcripts strongly accumulate following fungal elicitation. Challenged field roots containing functional ZmTps21 alleles displayed b-costic acid levels over 100 µg g-1 fresh weight, greatly exceeding in vitro concentrations required to inhibit the growth of five different fungal pathogens and rootworm larvae (Diabrotica balteata). In vivo disease resistance assays, using ZmTps21 and Zmtps21 near-isogenic lines, further support the endogenous antifungal role of selinene-derived metabolites. Involved in the biosynthesis of nonvolatile antibiotics, ZmTps21 exists as a useful gene for germplasm improvement programs targeting optimized biotic stress resistance.
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U2 - 10.1104/pp.17.00879
DO - 10.1104/pp.17.00879
M3 - Article
C2 - 28931629
AN - SCOPUS:85033786462
SN - 0032-0889
VL - 175
SP - 1455
EP - 1468
JO - Plant physiology
JF - Plant physiology
IS - 3
ER -