Allelic differences of clustered terpene synthases contribute to correlated intraspecific variation of floral and herbivory‐induced volatiles in a wild tobacco

Abstract

Plant volatile emissions can recruit predators of herbivores for indirect defense and attract pollinators to aid in pollination. Although volatiles involved in defense and pollinator attraction are primarily emitted from leaves and flowers, respectively, they will co-evolve if their underlying genetic basis is intrinsically linked, due either to pleiotropy or to genetic linkage. However, direct evidence of co-evolving defense and floral traits is scarce. We characterized intraspecific variation of herbivory-induced plant volatiles (HIPVs), the key components of indirect defense against herbivores, and floral volatiles in wild tobacco Nicotiana attenuata. We found that variation of (E)-b-ocimene and (E)-a-bergamotene contributed to the correlated changes in HIPVs and floral volatiles among N. attenuata natural accessions. Intraspecific variations of (E)-b-ocimene and (E)-a-bergamotene emissions resulted from allelic variation of two genetically co-localized terpene synthase genes, NaTPS25 and NaTPS38, respectively. Analyzing haplotypes of NaTPS25 and NaTPS38 revealed that allelic variations of NaTPS25 and NaTPS38 resulted in correlated changes of (E)-b-ocimene and (E)-a-bergamotene emission in HIPVs and floral volatiles in N. attenuata. Together, these results provide evidence that pleiotropy and genetic linkage result in correlated changes in defenses and floral signals in natural populations, and the evolution of plant volatiles is probably under diffuse selection.

Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco

“…during the day time (Fig. S1 ), consistent with previous findings [ 27 ]. Because plant volatiles play essential roles in mediating this tri-trophic interaction [ 23 , 26 ] and to get a better understanding of their diurnal/nocturnal regulation, we collected headspace day and night time volatiles from N. attenuata leaves on glasshouse-grown plants elicited by wounding plus M. sexta larval regurgitant (W + R) using PDMS tubing pieces (Kallenbach et al [ 30 ], Fig.…”

“…However, the same compound is nocturnally released from flowers and attracts adults of the same insect, which provides pollination services [ 24 ]. Further study showed that ( E )-β-ocimene and ( E )-α-bergamotene are correlated with each other across different N. attenuata genotypes, but linalool is independently regulated [ 23 , 27 ]. Furthermore, unlike the emission of linalool, the endogenous leaf pools of conjugates derived from linalool, such as linalool glycosides, lack the diurnal pattern of emissions [ 23 ].…”

“…However, when emitted from attacked leaves during the day, it attracts natural enemies of M. sexta larvae [ 24 ] to mediate a potent indirect defense [ 26 ]. The emission of ( E )-β-ocimene, produced by NaTPS25 , was correlated with ( E )-α-bergamotene emission from diverse N. attenuata accessions, and the two genes are co-localized on the N. attenuata genome [ 27 ]. In contrast, a QTL for the emission of linalool, a monoterpene produced by NaLIS , was mapped to a locus different from that of ( E )-α-bergamotene and ( E )-β-ocimene.…”

Comparative Metabolomics of Fruits and Leaves in a Hyperdiverse Lineage Suggests Fruits Are a Key Incubator of Phytochemical Diversification

“…Such a pathway has a limited capacity to generate organ-specific modifications of its end products prior to transport, and the sink organs may lack the metabolic machinery required for such modifications. Other secondary metabolites are locally synthesized, but in this case organ-specific metabolites derived from a shared metabolic pathway may be limited by genetic linkage, through co-localization of genes responsible for modifications within a metabolic pathway, e.g., terpene synthase clusters (Falara et al, 2011;Chen et al, 2020;Xu et al, 2020). Certainly, evolutionary processes may overcome these constraints when there are conflicting selection pressures among organs, as evidenced by the examples above of compounds occurring only in specific organs.…”

Comparative metabolomics of fruits and leaves in a hyperdiverse lineage suggests fruits are a key incubator of phytochemical diversification

“…Other secondary metabolites are locally synthesized, but in this case organspecific metabolites derived from a shared metabolic pathway may be limited by genetic linkage, through co-localization of genes responsible for modifications within a metabolic pathway, e.g. terpene synthase clusters (Falara et al, 2011;Chen et al, 2020;Xu et al, 2020). Certainly, evolutionary processes may overcome these constraints when there are conflicting selection pressures among organs, as evidenced by the numerous examples above of compounds occurring only in specific organs.…”