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Published on August 6, 2004; 10.1104/pp.104.044644

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Received April 15, 2004
Returned for revision June 10, 2004
Accepted June 14, 2004

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

Renato D'Ovidio , Alessandro Raiola , Cristina Capodicasa , Alessandra Devoto , 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.)

* Corresponding author; email: giulia.delorenzo{at}uniroma1.it.

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.




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