Influence of environmental temperature on mouth‐form plasticity in Pristionchus pacificus acts through daf‐11‐dependent cGMP signaling

Abstract

Mouth‐form plasticity in the nematode Pristionchus pacificus has become a powerful system to identify the genetic and molecular mechanisms associated with developmental (phenotypic) plasticity. In particular, the identification of developmental switch genes that can sense environmental stimuli and reprogram developmental processes has confirmed long‐standing evolutionary theory. However, how these genes are involved in the direct sensing of the environment, or if the switch genes act downstream of another, primary environmental sensing mechanism, remains currently unknown. Here, we study the influence of environmental temperature on mouth‐form plasticity. We find that environmental temperature does influence mouth‐form plasticity in most of the 10 wild isolates of P. pacificus tested in this study. We used one of these strains, P. pacificus RSA635, for detailed molecular analysis. Using forward and reverse genetic technology including CRISPR/Cas9, we show that mutations in the guanylyl cyclase Ppa‐daf‐11, the Ppa‐daf‐25/AnkMy2, and the cyclic nucleotide‐gated channel Ppa‐tax‐2 eliminate the response to elevated temperatures. Together, our study indicates that DAF‐11, DAF‐25, and TAX‐2 have been co‐opted for environmental sensing during mouth‐form plasticity regulation in P. pacificus.

Experimental and theoretical support for costs of plasticity and phenotype in a nematode cannibalistic trait

“…Specifically, the sulfatase-encoding eud-1 gene was identified as the key developmental switch that is regulated by various environmental factors and epigenetic mechanisms, and directs a downstream gene regulatory network consisting of more than 20 identified proteins including structural components of mouth formation ( Bui et al, 2018 ; Kieninger et al, 2016 ; Namdeo et al, 2018 ; Ragsdale et al, 2013 ; Sieriebriennikov et al, 2018 ; Sieriebriennikov et al, 2020 ; Sun et al, 2022 ). Importantly, worms respond to surrounding environmental cues to adopt their mouth form in a strain-specific manner, and various environmental stimuli, including temperature, culturing condition, crowding, and diet have been shown to influence mouth-morph ratios ( Lenuzzi et al, 2021 ; Werner et al, 2017 , 2018 ). Principally, three major features assist in studying P. pacificus mouth-form plasticity.…”

Linking Molecular Mechanisms and Evolutionary Consequences of Resource Polyphenism

“…Whether this expectation of evolutionary constraint is generalizable awaits additional empirical testing. One study addressing this issue, again in P. pacificus , found that phylogenetically conserved genes have been co-opted for temperature sensing as part of RP development (Lenuzzi et al, 2021 ). It is still unclear if this co-option involved the loss of ancestral functionality, a transition in functionality, or an addition to the functionality of these genes or their pathways.…”

“…Despite the growing evidence that evolution of plasticity might generally feature changes in effector genes, this issue is far from settled. We recall that the evolution of environmental sensing mechanisms (i.e., parts of the plastic response upstream of a developmental switch) in P. pacificus contributed to variation in temperature-dependent mouth form development (Lenuzzi et al, 2021 ). Moreover, the process of “building up” a polyphenism from a non-polyphenic ancestor likely requires more than a simple change to downstream effectors, as has been indicated by changes in regulatory genes themselves (Sieriebriennikov et al, 2018 ; Bhardwaj et al, 2020 ; Biddle and Ragsdale, 2020 ).…”

Experimental and theoretical support for costs of plasticity and phenotype in a nematode cannibalistic trait

“…Importantly, worms respond to surrounding environmental cues to adopt their mouth form in a strain-specific manner and various environmental stimuli, including temperature, culturing condition, crowding and diet have been shown to influence mouth-morph ratios [24][25][26].…”

“…Specifically, the sulfatase-encoding eud-1 gene was identified as the key developmental switch that is regulated by various environmental factors and epigenetic mechanisms, and directs a downstream gene regulatory network consisting of more than 20 identified proteins including structural components of mouth formation [17–23]. Importantly, worms respond to surrounding environmental cues to adopt their mouth form in a strain-specific manner and various environmental stimuli, including temperature, culturing condition, crowding and diet have been shown to influence mouth-morph ratios [24–26]. Principally, three major features assist in studying P. pacificus mouth-form plasticity.…”