Planta

, Volume 224, Issue 4, pp 750–760 | Cite as

Evolution of proteinase inhibitor defenses in North American allopolyploid species of Nicotiana

  • Jianqiang Wu
  • Christian Hettenhausen
  • Ian T. Baldwin
Original Article

Abstract

We studied the jasmonate (JA)-elicited trypsin-proteinase inhibitor (TPI) anti-herbivore defense system in North American Nicotiana to understand how complex polygenetic traits evolve after allopolyploidy speciation. N. quadrivalvis (Nq) and N. clevelandii (Nc) are allotetraploid descendant species of the ancestors of the diploid species N. attenuata (Na) and N. obtusifolia (No). From cDNA, intron and promoter sequence analyses, and Southern blotting, we deduced that only the maternally derived No TPI genes were retained in the tetraploid genomes (Nq, Nc), whereas the sequences of the paternal Na ancestor were deleted. The number of TPI repeats in different Nicotiana taxa was independent of phylogenetic associations. In Na, TPI activity and mRNA transcript accumulation as well as JA levels increased dramatically above wound-induced levels when the oral secretions (OS) from Manduca sexta larvae were introduced into wounds. This OS-mediated amplification of defense signaling and downstream response was also found in the tetraploid genomes but was absent from No; in No, OS treatment suppresses TPI mRNA accumulation and activity and does not increase JA accumulation. Hence, the tetraploids retained components of Na’s signaling system, but lost Na’s TPI genes and used No’s TPI genes to retain a functional TPI defense system, underscoring the genomic flexibility that enables complex polygenic traits to be retained in allopolyploid species.

Keywords

Nicotiana Plant–herbivore interaction Polygenic adaptation Polyploidy Proteinase inhibitor Solanaceae 

Abbreviations

ANOVA

Analysis of variance

HPLC-MS/MS

High-performance liquid chromatography coupled tandem mass spectrometry

ITS

Internal transcribed spacer

JA

Jasmonate

Na

Nicotiana attenuata

Nc

N. clevelandii

No

N. obtusifolia

Nq

N. quadrivalvis

OS

Oral secretions

TPI

Trypsin-proteinase inhibitor

Notes

Acknowledgements

We thank Max-Planck Gesellschaft and the Deutsche Forschungsgemeinschaft (SPP1152) for providing funding for this work.

Supplementary material

425_2006_256_MOESM1_ESM.pdf (196 kb)
Supplementary material

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Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Jianqiang Wu
    • 1
  • Christian Hettenhausen
    • 1
  • Ian T. Baldwin
    • 1
  1. 1.Department of Molecular EcologyMax-Planck-Institute for Chemical EcologyJenaGermany

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