Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana

Zhou, Wenwu; Brockmöller, Thomas; Ling, Zhihao; Omdahl, Ashton; Baldwin, Ian Thomas; Xu, Shuqing

doi:10.7554/elife.19531

Cited by 26 publications

(23 citation statements)

References 111 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…These results suggested that JA production or signal transduction is physiologically constrained in the “signal non-responsive” species. To test this hypothesis, we investigated the transcriptomes of 4 of the species ( N. attenuata , N. miersii , N. pauciflora and N. obtusifolia ) induced by W+W, W+OS Ms and W+OS Sl ( 53 ). Consistent with the pattern of metabolome reconfigurations, species were well-separated in the transcriptomic space with N. attenuata exhibited the highest OS-induced RDPI while N. obtusifolia being the lowest (Fig.…”

Section: Resultsmentioning

confidence: 99%

Information theory tests critical predictions of plant defense theory for specialized metabolism

Halitschke

Baldwin

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

1Different plant defense theories have provided important theoretical guidance in 2 explaining patterns in plant specialized metabolism, but their critical predictions remain to be 3 tested. Here, we systematically explored the metabolomes of Nicotiana attenuata, from single 4 plants to populations, as well as of closely-related species, using unbiased MS/MS analyses and 5 processed the abundances of compound-spectrum-based MS features within an information 6 theory framework to test critical predictions of Optimal Defense (OD) and Moving Target (MT) 7 theories. Information components of herbivory-elicited plant metabolomes were fully consistent 8 with the OD theory predictions and contradicted the main prediction of the MT theory. From 9 micro-to macro-evolutionary scales, jasmonate signaling was identified as the master 10 determinant of OD while ethylene signaling provided fine-tuning for herbivore-specific responses 11 annotated via MS/MS molecular networks. 12Plant defense theory, Information theory. 14 15 One-sentence summary: Information theory tests defense theory predictions by providing a 16 common currency for comparison of specialized metabolomes 17 Introduction 1 Structurally diverse specialized metabolites are central players in plants' adaptations to 2 their environments and in particular in their defense against enemies (1). The spectacular 3 diversification of specialized metabolism found in plants inspired several decades of intense 4 research about its multifaceted ecological functions and nucleated a long list of plant defense 5 theories that provided important guidance to empirical studies of the evolution and ecology of 6 plant-insect interactions (2). However, these plant defense theories did not follow the canonical 7 path of hypothetical-deductive reasoning in which critical predictions are posed at the same levels 8 of analysis (3) and tested experimentally to advance the next cycle of theory development (4).9Technical constraints limited data acquisition to specific metabolic classes and precluded the 10 comprehensive profiling of specialized metabolites and consequently, prevented the among-taxa 11 comparisons which were essential for theory advancement (5). This lack of comprehensive 12 metabolomics data and the processing workflows to compare the metabolic space among 13 different plant taxa in a common currency thwarted the scientific maturation of the field. 14 Recent advances in the field of tandem mass spectrometry (MS/MS) metabolomics are 15 allowing for comprehensive and high-throughput characterizations of metabolic variations within 16 and among species that comprise complete phylogenetic clades particularly when computational 17 methods are employed for the calculation of structural similarity among complex mixtures 18 without a priori chemical knowledge (5). This combination of analytical and computational 19advances provides the missing framework required for the rigorous testing of many predictions 20 made by the long-standing ecological and evolutionary theories on metab...

show abstract

Section: Resultsmentioning

confidence: 99%

Information theory tests critical predictions of plant defense theory for specialized metabolism

Halitschke

Baldwin

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…2C). Analyses on the herbivory-induced conserved transcriptomic responses in Nicotiana further showed that insertions of DTT-NIC1 are significantly enriched within the 1-kb upstream region of herbivory-induced early defense signaling genes in N. attenuata, and may have contributed to the recruitment of genes into the induced defense signaling network by introducing WRKY transcription factor binding sites (17).…”

Section: Resultsmentioning

confidence: 99%

Wild tobacco genomes reveal the evolution of nicotine biosynthesis

Brockmöller

Navarro‐Quezada

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

160

100

View full text Add to dashboard Cite

Nicotine, the signature alkaloid of Nicotiana species responsible for the addictive properties of human tobacco smoking, functions as a defensive neurotoxin against attacking herbivores. However, the evolution of the genetic features that contributed to the assembly of the nicotine biosynthetic pathway remains unknown. We sequenced and assembled genomes of two wild tobaccos, Nicotiana attenuata (2.5 Gb) and Nicotiana obtusifolia (1.5 Gb), two ecological models for investigating adaptive traits in nature. We show that after the Solanaceae whole-genome triplication event, a repertoire of rapidly expanding transposable elements (TEs) bloated these Nicotiana genomes, promoted expression divergences among duplicated genes, and contributed to the evolution of herbivoryinduced signaling and defenses, including nicotine biosynthesis. The biosynthetic machinery that allows for nicotine synthesis in the roots evolved from the stepwise duplications of two ancient primary metabolic pathways: the polyamine and nicotinamide adenine dinucleotide (NAD) pathways. In contrast to the duplication of the polyamine pathway that is shared among several solanaceous genera producing polyamine-derived tropane alkaloids, we found that lineage-specific duplications within the NAD pathway and the evolution of rootspecific expression of the duplicated Solanaceae-specific ethylene response factor that activates the expression of all nicotine biosynthetic genes resulted in the innovative and efficient production of nicotine in the genus Nicotiana. Transcription factor binding motifs derived from TEs may have contributed to the coexpression of nicotine biosynthetic pathway genes and coordinated the metabolic flux. Together, these results provide evidence that TEs and gene duplications facilitated the emergence of a key metabolic innovation relevant to plant fitness.Nicotiana genomes | genome-wide multiplications | transposable elements | nicotine biosynthesis | expression divergence

show abstract

“…The 44K 60-mer oligonucleotide microarrays designed for N. attenuata transcriptome analysis (Agilent) were used. cDNA preparation, hybridizations, and data analysis were performed as previously described (79). Probes were filtered by 1.5-fold change and adjusted P values are less than 0.05.…”

Section: Methodsmentioning

confidence: 99%

Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco

Wang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Optimal defense (OD) theory predicts that within a plant, tissues are defended in proportion to their fitness value and risk of predation. The fitness value of leaves varies greatly and leaves are protected by jasmonate (JA)-inducible defenses. Flowers are vehicles of Darwinian fitness in flowering plants and are attacked by herbivores and pathogens, but how they are defended is rarely investigated. We used Nicotiana attenuata, an ecological model plant with well-characterized herbivore interactions to characterize defense responses in flowers. Early floral stages constitutively accumulate greater amounts of two well-characterized defensive compounds, the volatile (E)-α-bergamotene and trypsin proteinase inhibitors (TPIs), which are also found in herbivore-induced leaves. Plants rendered deficient in JA biosynthesis or perception by RNA interference had significantly attenuated floral accumulations of defensive compounds known to be regulated by JA in leaves. By RNA-seq, we found a JAZ gene, NaJAZi, specifically expressed in early-stage floral tissues. Gene silencing revealed that NaJAZi functions as a flower-specific jasmonate repressor that regulates JAs, (E)-α-bergamotene, TPIs, and a defensin. Flowers silenced in NaJAZi are more resistant to tobacco budworm attack, a florivore. When the defensin was ectopically expressed in leaves, performance of Manduca sexta larvae, a folivore, decreased. NaJAZi physically interacts with a newly identified NINJA-like protein, but not the canonical NINJA. This NINJA-like recruits the corepressor TOPLESS that contributes to the suppressive function of NaJAZi on floral defenses. This study uncovers the defensive function of JA signaling in flowers, which includes components that tailor JA signaling to provide flower-specific defense

show abstract

Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana

Cited by 26 publications

References 111 publications

Information theory tests critical predictions of plant defense theory for specialized metabolism

Information theory tests critical predictions of plant defense theory for specialized metabolism

Wild tobacco genomes reveal the evolution of nicotine biosynthesis

Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco

Contact Info

Product

Resources

About