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Research Article

Plant immunity triggered by engineered in vivo release of oligogalacturonides, damage-associated molecular patterns

Manuel Benedetti, Daniela Pontiggia, Sara Raggi, Zhenyu Cheng, Flavio Scaloni, Simone Ferrari, Frederick M. Ausubel, Felice Cervone, and Giulia De Lorenzo
PNAS April 28, 2015 112 (17) 5533-5538; first published April 13, 2015; https://doi.org/10.1073/pnas.1504154112
Manuel Benedetti
aDepartment of Biology and Biotechnology “Charles Darwin,” Sapienza University of Rome, 00185 Rome, Italy;
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Daniela Pontiggia
aDepartment of Biology and Biotechnology “Charles Darwin,” Sapienza University of Rome, 00185 Rome, Italy;
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Sara Raggi
aDepartment of Biology and Biotechnology “Charles Darwin,” Sapienza University of Rome, 00185 Rome, Italy;
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Zhenyu Cheng
bDepartment of Genetics, Harvard Medical School, Boston, MA 02114; and
cDepartment of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114
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Flavio Scaloni
aDepartment of Biology and Biotechnology “Charles Darwin,” Sapienza University of Rome, 00185 Rome, Italy;
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Simone Ferrari
aDepartment of Biology and Biotechnology “Charles Darwin,” Sapienza University of Rome, 00185 Rome, Italy;
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Frederick M. Ausubel
bDepartment of Genetics, Harvard Medical School, Boston, MA 02114; and
cDepartment of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114
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  • For correspondence: ausubel@molbio.mgh.harvard.edu felice.cervone@uniroma1.it
Felice Cervone
aDepartment of Biology and Biotechnology “Charles Darwin,” Sapienza University of Rome, 00185 Rome, Italy;
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  • For correspondence: ausubel@molbio.mgh.harvard.edu felice.cervone@uniroma1.it
Giulia De Lorenzo
aDepartment of Biology and Biotechnology “Charles Darwin,” Sapienza University of Rome, 00185 Rome, Italy;
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  1. Contributed by Frederick M. Ausubel, March 10, 2015 (sent for review May 10, 2014; reviewed by Michael G. Hahn and Jonathan D. G. Jones)

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Significance

Damage-associated molecular patterns (DAMPs), released from host tissues as a consequence of pathogen attack, have been proposed as endogenous activators of immune responses in both animals and plants. Oligogalacturonides (OGs), oligomers of α-1,4–linked galacturonic acid generated in vitro by the partial hydrolysis of pectin, have been shown to function as potent elicitors of immunity when they are applied exogenously to plant tissues. However, there is no direct evidence that OGs can be produced in vivo or that they function as immune elicitors. This report provides the missing evidence that OGs can be generated in planta and can function as DAMPs in the activation of plant immunity.

Abstract

Oligogalacturonides (OGs) are fragments of pectin that activate plant innate immunity by functioning as damage-associated molecular patterns (DAMPs). We set out to test the hypothesis that OGs are generated in planta by partial inhibition of pathogen-encoded polygalacturonases (PGs). A gene encoding a fungal PG was fused with a gene encoding a plant polygalacturonase-inhibiting protein (PGIP) and expressed in transgenic Arabidopsis plants. We show that expression of the PGIP–PG chimera results in the in vivo production of OGs that can be detected by mass spectrometric analysis. Transgenic plants expressing the chimera under control of a pathogen-inducible promoter are more resistant to the phytopathogens Botrytis cinerea, Pectobacterium carotovorum, and Pseudomonas syringae. These data provide strong evidence for the hypothesis that OGs released in vivo act as a DAMP signal to trigger plant immunity and suggest that controlled release of these molecules upon infection may be a valuable tool to protect plants against infectious diseases. On the other hand, elevated levels of expression of the chimera cause the accumulation of salicylic acid, reduced growth, and eventually lead to plant death, consistent with the current notion that trade-off occurs between growth and defense.

  • plant immunity
  • DAMPs
  • polygalacturonase
  • PGIP
  • oligogalacturonides

Footnotes

  • ↵1To whom correspondence may be addressed. Email: ausubel{at}molbio.mgh.harvard.edu or felice.cervone{at}uniroma1.it.
  • Author contributions: M.B., S.F., F.C., and G.D.L. designed research; M.B., D.P., S.R., Z.C., F.S., and S.F. performed research; M.B., D.P., S.R., Z.C., S.F., F.M.A., F.C., and G.D.L. analyzed data; M.B., D.P., S.F., F.M.A., F.C., and G.D.L. wrote the paper; and F.M.A., F.C., and G.D.L. supervised the project.

  • Reviewers: M.G.H., University of Georgia; and J.D.G.J., Sainsbury Laboratory.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1504154112/-/DCSupplemental.

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Engineering DAMP release in Arabidopsis
Manuel Benedetti, Daniela Pontiggia, Sara Raggi, Zhenyu Cheng, Flavio Scaloni, Simone Ferrari, Frederick M. Ausubel, Felice Cervone, Giulia De Lorenzo
Proceedings of the National Academy of Sciences Apr 2015, 112 (17) 5533-5538; DOI: 10.1073/pnas.1504154112

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Engineering DAMP release in Arabidopsis
Manuel Benedetti, Daniela Pontiggia, Sara Raggi, Zhenyu Cheng, Flavio Scaloni, Simone Ferrari, Frederick M. Ausubel, Felice Cervone, Giulia De Lorenzo
Proceedings of the National Academy of Sciences Apr 2015, 112 (17) 5533-5538; DOI: 10.1073/pnas.1504154112
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Proceedings of the National Academy of Sciences: 112 (17)
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