Middle <scp>D</scp>evonian liverwort herbivory and antiherbivore defence

Labandeira, Conrad C.; Tremblay, Susan; Bartowski, Kenneth E.; Hernick, Linda VanAller

doi:10.1111/nph.12643

Cited by 72 publications

(43 citation statements)

References 86 publications

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“…mites), external feeding damage in fossil leaves from these studies was attributed to mandibulate insects based on the recurrence of subsurface mouthpart marks, avoidance of indurated leaf structures (cell walls, lignified tissues), and reaction rims. Although it is possible that non-arthropod invertebrates such as pulmonate snails and slugs, may have inflicted some of the observed leaf-chewing damage, their radulae leave marks that cannot be confused with those of mandibulate arthropods [40].…”

Section: Methodsmentioning

confidence: 99%

Insect Leaf-Chewing Damage Tracks Herbivore Richness in Modern and Ancient Forests

et al. 2014

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The fossil record demonstrates that past climate changes and extinctions significantly affected the diversity of insect leaf-feeding damage, implying that the richness of damage types reflects that of the unsampled damage makers, and that the two are correlated through time. However, this relationship has not been quantified for living leaf-chewing insects, whose richness and mouthpart convergence have obscured their value for understanding past and present herbivore diversity. We hypothesized that the correlation of leaf-chewing damage types (DTs) and damage maker richness is directly observable in living forests. Using canopy access cranes at two lowland tropical rainforest sites in Panamá to survey 24 host-plant species, we found significant correlations between the numbers of leaf chewing insect species collected and the numbers of DTs observed to be made by the same species in feeding experiments, strongly supporting our hypothesis. Damage type richness was largely driven by insect species that make multiple DTs. Also, the rank-order abundances of DTs recorded at the Panamá sites and across a set of latest Cretaceous to middle Eocene fossil floras were highly correlated, indicating remarkable consistency of feeding-mode distributions through time. Most fossil and modern host-plant pairs displayed high similarity indices for their leaf-chewing DTs, but informative differences and trends in fossil damage composition became apparent when endophytic damage was included. Our results greatly expand the potential of insect-mediated leaf damage for interpreting insect herbivore richness and compositional heterogeneity from fossil floras and, equally promisingly, in living forests.

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Section: Methodsmentioning

confidence: 99%

Insect Leaf-Chewing Damage Tracks Herbivore Richness in Modern and Ancient Forests

et al. 2014

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“…In addition, a role against herbivory was postulated by Stahl, who presented snails with fresh or alcohol-leached liverworts and noted that snails preferred the latter and did not consume the former to any extent [26]. An anti-herbivory role is also supported by fossilized evidence of herbivore oil body avoidance in Devonian liverworts [27]. Furthermore, the chemical constituents of oil bodies lead to growth inhibition of bacterial and fungal pathogens [28-32].…”

Section: Introductionmentioning

confidence: 99%

Oil body formation inMarchantia polymorphais controlled by MpC1HDZ and serves as a defense against arthropod herbivores

Romani

Banić

Florent

et al. 2020

Preprint

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26 27 28 SUMMARY 29 The origin of a terrestrial flora in the Ordovician required adaptation to novel biotic and abiotic 30 stressors. Oil bodies, a synapomorphy of liverworts, accumulate secondary metabolites, but their 31 function and development are poorly understood. Oil bodies of Marchantia polymorpha develop 32 within specialized cells as one single large organelle. Here, we show that a CLASS I 33 HOMEODOMAIN LEUCINE-ZIPPER (C1HDZ) transcription factor controls the differentiation of 34 oil body cells in two different ecotypes of the liverwort M. polymorpha, a model genetic system for 35 early divergent land plants. In flowering plants, these transcription factors primarily modulate 36 responses to abiotic stresss including drought. However, loss-of-function alleles of the single ortholog 37 gene, MpC1HDZ, in M. polymorpha did not exhibit phenotypes associated with abiotic stress. Rather 38 Mpc1hdz mutant plants were more susceptible to herbivory and total plant extracts of the mutant 39 exhibited reduced antibacterial activity. Transcriptomic analysis of the mutant revealed a reduction 40 in expression of genes related to secondary metabolism that was accompanied by a specific depletion 41 of oil body terpenoid compounds. Through time lapse imaging we observed that MpC1HDZ 42 expression maxima precede oil body formation indicating that MpC1HDZ mediates differentiation 43 of oil body cells. Our results indicate that M. polymorpha oil bodies, and MpC1HDZ, are critical for 44 defense against herbivory but not for abiotic stress-tolerance. Thus, C1HDZ genes were co-opted to 45 regulate separate responses to biotic and abiotic stressors in two distinct land plant lineages.46 47 48 49 The emergence of land flora in the Ordovician and the subsequent radiation of plants into terrestrial 50 environments were major evolutionary events in the history of Earth. This radical breakthrough for 51 life on the planet entailed the evolution of both new developmental programs and biochemical 52 pathways [1]. Early land plants were faced with novel biotic and abiotic stressors, including a 53 desiccating aerial environment, increased solar radiation, and greater interspecific competition, 54 including herbivory. This transition was accompanied by a dramatic increase in the diversity of 55 secondary metabolites and the complexity of transcriptional regulation, to protect plants from 56 herbivores and pathogens, and also abiotic stressors such as desiccation and light intensity [2-4]. 57 Liverworts represent one of the earliest diverging land plant lineages, with a predicted Ordovician-58 Silurian origin of all three major extant liverwort clades [5, 6]. One synapomorphy of this lineage is 59 the presence of oil bodies, specialized organelles containing an array of lipophilic secondary 60 compounds [7]. In some liverworts, multiple oil bodies are found in nearly all differentiated cells of 61 both gametophyte and sporophyte generations. Whilst in other liverworts, such as Marchantia 62 polymorpha (M. polymorpha), oil bodies are ...

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“…, Banks and Colthart ) and lamina‐like organs of liverworts (Labandeira et al. ). Liverworts do not possess true leaves, but rather consist of a green gametophytic thallus, unlike vascular plant sporophytes with megaphylls.…”

Section: Introductionmentioning

confidence: 99%

“…However, since Labandeira's () publication, additional functional feeding groups from geologic deep past have been found; for instance, Labandeira et al. () described Phase 1 galls in Metzgeriothallus sharonae from the Middle Devonian.…”

Section: Introductionmentioning

confidence: 99%

“…The fourth phase arrives considerably later and represents the consumption of angiosperm host plants, and the development of associations overwhelmingly with derived lineages of hemipteroid and holometabolous insect orders. However, since Labandeira's (2006) publication, additional functional feeding groups from geologic deep past have been found; for instance, Labandeira et al (2014) described Phase 1 galls in Metzgeriothallus sharonae from the Middle Devonian.…”

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Insect herbivory fluctuations through geological time

Pinheiro

Iannuzzi

Duarte

2016

Ecology

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Arthropods and land plants are the major macroscopic sources of biodiversity on the planet. Knowledge of the organization and specialization of plant-herbivore interactions, such as their roles in food webs is important for understanding the processes for maintaining biodiversity. A limited number of studies have examined herbivory through geological time. The most have analyzed localities from one restricted interval within a geological period, or a time transition such as the Paleocene-Eocene boundary interval. In the present study, we analyzed the frequency of herbivory and density of damage type (DT) from the Middle Devonian to the early Miocene. The data were compiled from literature sources and focused on studies that describe occurrences of leaves with DTs indicating herbivore consumption as a proportion of the total number of leaves analyzed. The data were standardized based on the DT categories in the Damage Type Guide, and the age of each locality was updated based on the most recent geochronological standard and expressed in millions of years. Temperature and geological age were the best descriptors of the variation in herbivory frequency, which tended to increase at higher temperatures. Two models were equivalent to explain DT density: the interaction between CO levels and geological age, and O levels and geological age had the same predictive power. The density of DT tended to increase with higher content of atmospheric CO and O compared to modern values. The frequency of herbivory and the density of DTs appear to be influenced by long-term atmospheric variables.

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Middle Devonian liverwort herbivory and antiherbivore defence

Cited by 72 publications

References 86 publications

Insect Leaf-Chewing Damage Tracks Herbivore Richness in Modern and Ancient Forests

Insect Leaf-Chewing Damage Tracks Herbivore Richness in Modern and Ancient Forests

Oil body formation inMarchantia polymorphais controlled by MpC1HDZ and serves as a defense against arthropod herbivores

Insect herbivory fluctuations through geological time

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