Science - USA (2022-02-04)

RESEARCH ARTICLE SUMMARY

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PLANT SCIENCE

Natural historyÐguided omics reveals plant defensive

chemistry against leafhopper pests

Yuechen Bai, Caiqiong Yang, Rayko Halitschke, Christian Paetz, Danny Kessler, Konrad Burkard,
Emmanuel Gaquerel, Ian T. Baldwin, Dapeng Li*

INTRODUCTION:Although much is known about
plant traits that function in nonhost resistance
against pathogens, little is known about non-
host resistance against herbivores, despite its
agricultural importance, because of the lack
of fieldwork.Empoascaleafhoppers, serious
agricultural pests, identify host plants by eaves-
dropping on unknown outputs of jasmonate
(JA)–mediated signaling in a native tobacco
plant that is naturally variable in its JA signal-
ing. The known sectors of this tobacco plant’s
specialized defense metabolism are not effec-
tive against this insect, which calls for an un-
biased approach.

RATIONALE:An unbiased forward-genetics ap-
proach based on the screening of a 26-parent
recombinant inbred line population in a

natural habitat with native herbivores was

weddedwithunbiasedtranscriptomicand

mass spectrometry–based metabolomic analy-

ses of reverse-genetics lines to identify defense

chemistries produced by this native tobacco

when probed by leafhoppers. Synthetic biology

approaches were used to reconstitute these

chemistries in crop plants.

RESULTS:The analysis revealed anEmpoasca-

elicited JA-JAZi module that pointed to the

phenolamide master transcription factor,

MYB8, as a central genetic hub clustering with

putrescine-derived phenolamides. Using to-

bacco plants silenced for components of JA sig-

naling (JAZandMYC2genes) and phenolamide

biosynthesis, the central role of a MYC2-MYB8-

JAZi branch of JA signaling was confirmed;

however, infiltration ofMYC2-silenced plants

with known putrescine-derived phenolamides

did not alterEmpoascapreference. Subse-

quent detailed structural analysis revealed an

unknown metabolite whose abundance was

regulated by the MYC2-MYB8-JAZi branch of

JA signaling and was negatively correlated with

Empoascadamage. Previous work on this un-

known metabolite suggested a conjugate of

caffeoylputrescine with a C-6 aldehyde produced

during wound-induced lipid peroxidation—a

process that leads to the formation of green

leaf volatiles. Metabolite quantitative trait locus

(mQTL) analysis and coexpression analysis

pointed to two polyphenol oxidases (PPOs)

and one berberine bridge enzyme-like 2 (BBL2)

gene associated with the metabolite’s bio-

synthesis. The function of the proteins encoded

by these genes was tested in both in vitro

[Escherichia coliexpression and enzymatic as-

says with (Z)-3-hexenal and caffeoylputrescine]

and in vivo (transient expression inSolanum

chilenseandVicia faba) systems. The structure

of the unknown metabolite was identified by

nuclear magnetic resonance (NMR) to be a

caffeoylputrescine–green leaf volatile com-

pound (CPH), catalyzed by a PPO in a Michael

addition reaction and requiring BBL2 in planta.

Synthetic biology approaches confirmed the

function of CPH in nonhost resistance against

Empoascaleafhoppers inNicotiana attenuata

lines silenced to be defective in CPH production;

inV. faba, a bean crop host plant of the leaf-

hoppers unable to produce caffeoylputrescine;

and inS. chilense.

CONCLUSION:The natural history–driven multi-

omics framework used for the discovery of

CPH and its marriage with synthetic biology

approaches highlight how readily the results

of millions of years of innovation by natural

selection can be amortized and transferred

to crop plants to catalyze a greener and eco-

logically more nuanced revolution in plant

protection. Crop plants face challenges not

substantially different from those faced by

native plants; they are constantly tested by

hidden herbivore communities that challenge

the host-nonhost distinction. In a world of

climate change and globally homogenized

herbivore communities, opportunistic associ-

ations will dominate natural and man-made

ecosystems. CPH represents a chemical inno-

vation that allows a native plant to cope with

these opportunistic associations and is readily

engineered in crop plants.▪

RESEARCH

514 4 FEBRUARY 2022•VOL 375 ISSUE 6580 science.orgSCIENCE

The list of author affiliations is available in the full article online.

*Corresponding author. Email: [email protected] (Y.B.);

[email protected] (I.T.B.); [email protected] (D.L.)

Cite this article as Y. Baiet al.,Science 375 , eabm2948

(2022). DOI: 10.1126/science.abm2948

READ THE FULL ARTICLE AT

https://doi.org/10.1126/science.abm2948

JAZi

MYC2

MYB8

• 
  

O

NH

NH 2

OH

HO

CH 3

O

Caffeoyl-CoA

Co A

O

S

OH

HO

NH 2

H 2 N

Putrescine

O

(Z)-3-hexenal

PPO1

PPO2

BBL2

Michael addition

AT1

CPHCPH

CP

Green-leaf-volatile pathway Phenylpropanoid pathway Polyamine pathway

Jasmonate signaling

HO

Opportunistic leafhopper attack elicits caffeoylputrescineÐgreen leaf volatile defenses.Attack elicits a
JAZi-mediated sector of JA signaling to condense the products of three branches of specialized metabolism
(green leaf volatile, phenylpropanoid, and polyamine pathways) in a native tobacco plant through a PPO-catalyzed
and BBL2-mediated Michael addition reaction to produce previously unobserved defense chemistry (CPH) that
was reconstituted in crop plants for durable nonhost resistance. CP, caffeoylputrescine; AT1, acyltransferase 1.