Innovation in anti‐herbivore defense systems during neopolypoloidy – the functional consequences of instantaneous speciation

Abstract

SummaryAllopolyploid hybridization instantly merges two differentially adapted genomes into one individual. Allopolyploids are often evolutionarily successful, undergoing adaptive radiations despite the genetic and physiological challenges of merging genomes. We examine a suite of induced herbivore resistance traits in three independent lines of the synthetic allopolyploid Nicotiana · mierata (Nma) and its parent species, N. miersii (Nmi) and N. attenuata (Na), to determine how a complex polygenetic adaptation fares during the early stages of neoallopolyploid formation. All species responded to Manduca sexta oral secretions (OS) with a temporally prolonged jasmonate (JA) burst. In one parent (Na), the JA burst was additionally amplified and associated with the elicitation of direct and indirect defenses. In the other parent (Nmi), OS neither amplified the JA burst nor elicited defense responses, although applied MeJA confirmed the inducibility of the defense responses. All lines of Nma retained enough aspects of Na's JA signaling to recognize OS and to accumulate sufficient direct defenses to impair the growth of Manduca larvae. Most defense-related metabolites were retained in Nma even if inherited from only one parent; however, OS-elicited volatiles, trypsin protease inhibitors (TPIs) and chlorogenic acid were lost in some lines, even though MeJA treatment elicited similar responses in all lines. Herbivore defense systems are flexibly inherited in allopolyploids, causing individuals to diverge over only a few generations; for example, line 1 of Nma could not produce TPIs after OS elicitation, whereas lines 2 and 3 could. This flexible integration of defense signaling systems with a diversity of elicited responses may explain why adaptive radiations are commonly found in allopolyploid lineages.

The predictability of traits and ecological interactions on 17 different crosses of hybrid oaks

“…The breakdown of defensive systems in hybrids has received little attention from plant physiologists. However, metabolic screens of plant secondary compounds, which often play a defensive role against herbivore attack, have revealed unexpected patterns of inheritance in hybrid plants (Orians and Fritz 1995;Orians 2000;Pearse et al 2006;Yarnes et al 2008). In terms of hybrid outbreeding depression in animals, hybrids produced from parental species that are less related to one another are less Wt than hybrids produced from phylogenetically close relatives, as divergent evolutionary history is a good proxy for the divergence of physiological systems (Coyne and Orr 1989).…”

Variation in Antiherbivore Defense Responses in Synthetic Nicotiana Allopolyploids Correlates with Changes in Uniparental Patterns of Gene Expression

“…The last decade witnessed impressive advances in polyploidy research, with new results from Arabidopsis (Comai et al, 2000;Pontes et al, 2004), Brassica species (Lukens et al, 2006;Gaeta et al, 2007), cotton (Jiang et al, 1998), wheat (Han et al, 2003), and Nicotiana species (Lim et al, 2006;Pearse et al, 2006;Anssour et al, 2009). Most of these studies have focused on the genetic and genomic changes associated with the formation of polyploids, especially changes directly altering gene expression patterns, such as rapid and nonrandom changes including sequence elimination, changes in the DNA loci, and intergenomic cross talk, for example, transposon activation, chromosomal rearrangements, and chromosomal breaks (Kenton et al, 1993;Kitamura et al, 1997;Chase et al, 2003;Lim et al, 2004;Leitch et al, 2008).…”

“…The first attempts, carried out by Pearse et al (2006), to synthesize Na and No allopoylploids were unsuccessful, thus the authors used Nicotiana miersii as a maternal surrogate for No (the species most phylogenetically related to No) to create the synthetic neoallopolyploid, Nicotiana 3 mierata. By eliciting plants with OS and methyl jasmonate (MeJA) and comparing the changes in TPI activity, secondary metabolites, and released volatile organic compounds in the parents with those of the neoallopolyploid lines, the authors concluded that parental signaling cascades eliciting these defense responses had been reshuffled in the neopolyploids in a plug-and-play fashion to allow different secondary metabolite responses to be elicited by the diversity of OS-and JA-elicited signaling systems found in the parents.…”

Evolution of physiological responses to salt stress in hexaploid wheat

“…For example, Coate et al (6) showed that tolerance to chronic light stress was significantly increased in a newly formed allotetraploid of soybean (Glycine dolichocarpa) compared with its diploid progenitors. Neoallopolyploid tobacco (Nicotiana miersii × Nicotiana attenuata) showed an innovation of defense against herbivores (7). Both natural and artificial Arabidopsis tetraploids exhibit higher potassium uptake and salinity tolerance than their diploid counterparts (8).…”