Plant Physiol.
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First published online August 6, 2004; 10.1104/pp.104.044644

Plant Physiology 135:2424-2435 (2004)
© 2004 American Society of Plant Biologists

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Characterization of the Complex Locus of Bean Encoding Polygalacturonase-Inhibiting Proteins Reveals Subfunctionalization for Defense against Fungi and Insects1

Renato D'Ovidio2, Alessandro Raiola2,3, Cristina Capodicasa2, Alessandra Devoto2,4, Daniela Pontiggia, Serena Roberti, Roberta Galletti, Eric Conti, Donal O'Sullivan and Giulia De Lorenzo*

Dipartimento di Agrobiologia e Agrochimica, Università della Tuscia, 01100 Viterbo, Italy (R.D., C.C., S.R.); Dipartimento di Biologia Vegetale, Università di Roma La Sapienza, 00185 Rome, Italy (A.R., A.D., D.P., R.G., G.D.L.); Dipartimento di Arboricoltura e Protezione delle Piante – Entomologia, Università di Perugia, 06121 Perugia, Italy (E.C.); and National Institute of Agricultural Botany, Cambridge CB3 0LE, United Kingdom (D.O.)

Polygalacturonase-inhibiting proteins (PGIPs) are extracellular plant inhibitors of fungal endopolygalacturonases (PGs) that belong to the superfamily of Leu-rich repeat proteins. We have characterized the full complement of pgip genes in the bean (Phaseolus vulgaris) genotype BAT93. This comprises four clustered members that span a 50-kb region and, based on their similarity, form two pairs (Pvpgip1/Pvpgip2 and Pvpgip3/Pvpgip4). Characterization of the encoded products revealed both partial redundancy and subfunctionalization against fungal-derived PGs. Notably, the pair PvPGIP3/PvPGIP4 also inhibited PGs of two mirid bugs (Lygus rugulipennis and Adelphocoris lineolatus). Characterization of Pvpgip genes of Pinto bean showed variations limited to single synonymous substitutions or small deletions. A three-amino acid deletion encompassing a residue previously identified as crucial for recognition of PG of Fusarium moniliforme was responsible for the inability of BAT93 PvPGIP2 to inhibit this enzyme. Consistent with the large variations observed in the promoter sequences, reverse transcription-PCR expression analysis revealed that the different family members differentially respond to elicitors, wounding, and salicylic acid. We conclude that both biochemical and regulatory redundancy and subfunctionalization of pgip genes are important for the adaptation of plants to pathogenic fungi and phytophagous insects.


1 This work was supported by the Giovanni Armenise-Harvard Foundation, by MIUR (Ministero dell'Istruzione, dell'Università e della Ricerca; grants PRIN [Programmi di Ricerca Scientifica di Rilevante Interesse Nazionale] 2002 and FIRB [Fondo per gli Investimenti della Ricerca di Base] 2001), by the Institute Pasteur-Fondazione Cenci Bolognetti, and by European Community Grants (grant nos. ICA4–CT–2000–30033 and QLK1–CT–2000–00811).

2 These authors contributed equally to the paper.

3 Present address: Dipartimento Territorio e Sistemi Agro-Forestali, Sezione Patologia Vegetale, Università degli Studi di Padova, Viale dell'Università 23, 35020 Legnaro (PD), Italy.

4 Present address: University of East Anglia, School of Biological Science, Norwich NR4 7TJ, UK.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.044644.

* Corresponding author; e-mail giulia.delorenzo{at}uniroma1.it; fax 390649912446.

Received April 15, 2004; returned for revision June 10, 2004; accepted June 14, 2004.




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