On the Origin of Carnivory: Molecular Physiology and Evolution of Plants on an Animal Diet

Abstract

Charles Darwin recognized that carnivorous plants thrive in nutrient-poor soil by capturing animals. Although the concept of botanical carnivory has been known for nearly 150 years, its molecular mechanisms and evolutionary origins have not been well understood until recently. In the last decade, technical advances have fueled the genome and transcriptome sequencings of active and passive hunters, leading to a better understanding of the traits associated with the carnivorous syndrome, from trap leaf development and prey digestion to nutrient absorption, exemplified by the Venus flytrap ( Dionaea muscipula), pitcher plant ( Cephalotus follicularis), and bladderwort ( Utricularia gibba). The repurposing of defense-related genes is an important trend in the evolution of plant carnivory. In this review, using the Venus flytrap as a representative of the carnivorous plants, we summarize the molecular mechanisms underlying their ability to attract, trap, and digest prey and discuss the origins of plant carnivory in relation to their genomic evolution. Expected final online publication date for the Annual Review of Plant Biology, Volume 72 is May 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Integration of electric, calcium, reactive oxygen species and hydraulic signals during rapid systemic signaling in plants

“…These measurements indicate that the local application of HL stress or wounding resulted in the triggering of systemic membrane depolarization changes that spread through the entire plant. APs and VPs were previously reported in response to a local treatment of wounding or HL stress in Arabidopsis, supporting the results presented here (Farmer et al ., 2020; Hedrich and Fukushima, 2021; Mousavi et al ., 2013; Nguyen et al ., 2018; Shao et al ., 2020; Szechyńska‐Hebda et al ., 2010). In contrast to the responses measured in wild‐type plants, systemic changes in membrane potential were not observed in the rbohD , glr3.3;glr3.6 or pdlp5 mutants in response to local application of HL or wounding (Figure 3).…”

“…The dye‐based, fumigation‐applied, whole‐plant live ROS imaging method we developed (Fichman et al ., 2019) has been validated in different studies using different mutants (Fichman et al ., 2020; Fichman et al ., 2021; Zandalinas et al ., 2020a), omics tools (Choudhury et al ., 2018; Zandalinas et al ., 2019; Zandalinas et al ., 2020a) and, more recently, whole‐plant imaging of transgenic plants with stable expression of cytosolic reduction‐oxidation sensitive green fluorescent protein 1 (roGFP1; Fichman and Mittler, 2021). Although the dye‐based, fumigation‐applied, whole‐plant live imaging methods developed and utilized in our current study to image systemic changes in calcium levels and membrane potential (Figures 2 and 3) may not be ideal to study the short‐term kinetics of changes in membrane potential and subcellular calcium levels, as are measurements of systemic electric signals using different electrodes (e.g., Farmer et al ., 2020; Hedrich and Fukushima, 2021), or the use of transgenic plants with stable expression of different ratiometric sensor proteins for measuring changes in calcium levels in different subcellular compartments (e.g., Toyota et al ., 2018), they are nevertheless ideal for studying the overall process of systemic signal activation in different mutants, and could prove valuable for future large‐scale screens of different mutant populations. For such studies the short‐term kinetics of systemic signal propagation is not as important as the answer to whether or not a systemic signal is turned “on” in different mutants (Figures 2 and 3).…”

“…Because plants lack a nervous system that connects the sensing (i.e., local) tissue with all other plant tissues that did not yet experience the stress/pathogen/stimuli (i.e., systemic tissues), systemic signals in plants must travel from cell‐to‐cell over long distances, sometimes spanning the entire length of the plant (Choi et al ., 2017; Farmer et al ., 2020; Fichman and Mittler, 2020b; Johns et al ., 2021; Mittler et al ., 2011; Vega‐Muñoz et al ., 2020). Among the different signaling processes thought to mediate such rapid long distance cell‐to‐cell signal transduction mechanisms in plants are changes in membrane potentials (i.e., electric waves; Farmer et al ., 2020; Hedrich and Fukushima, 2021; Mousavi et al ., 2013; Nguyen et al ., 2018; Shao et al ., 2020; Szechyńska‐Hebda et al ., 2010), steady‐state levels of calcium (i.e., calcium wave; Choi et al ., 2014; Choi et al ., 2017; Dubiella et al ., 2013; Evans et al ., 2016; Shao et al ., 2020; Tian et al ., 2020; Toyota et al ., 2018), steady‐state levels of reactive oxygen species (ROS; i.e., ROS wave; Fichman et al ., 2019; Fichman and Mittler, 2020b; Kollist et al ., 2019; Lew et al ., 2020; Miller et al ., 2009; Mittler et al ., 2011; Zandalinas et al ., 2019; Zandalinas et al ., 2020a; Zandalinas et al ., 2020b), hydraulic pressure (i.e., hydraulic wave; Christmann et al ., 2013; Malone, 1992; Sade et al ., 2014), as well as rapid changes in the levels of different plant hormones such as jasmonic acid (JA), abscisic acid (ABA) and auxin (Devireddy et al ., 2018; Galvez‐Valdivieso et al ., 2009; Guo et al ., 2016; Kangasjärvi et al ., 2009; Wang et al ., 2019), small peptides (Takahashi et al ., 2018), redox levels (Fichman and Mittler, 2021), and/or different metabolites/metabolic signatures (Choudhury et al ., 2018). Recent studies demonstrated that many of these signals propagate from cell‐to‐cell through the vascular bundles of plants using tissues such as xylem parenchyma and phloem cells to mediate systemic electric, calcium and ROS signals, and xylem cells to mediate hydraulic pressure signals (Ch...…”

Ether anesthetics prevents touch-induced trigger hair calcium-electrical signals excite the Venus flytrap

“…MSL10 type channels in Arabidopsis and Dionaea operate as anion channels that upon activation depolarize cells (Maksaev and Haswell, 2012), while OSCAs rather Ca 2+ (Yuan et al, 2014, Murthy et al, 2018, Thor et al, 2020. To trigger excitation in the flytrap cells have to be depolarized by 20-40 mV from the resting state (Hedrich and Fukushima, 2021). Thus, together MSL10 and OSCA(s) likely give rise to depolarization and Ca 2+ influx for activation of anion channels.…”

Ether Anesthetics Obstructs Touch-Induced Trigger Hair Calcium-Electrical Signals Preventing Excitation of The Venus Flytrap

“…MSL10 type channels in Arabidopsis and Dionaea operate as anion channels that upon activation depolarize cells (Maksaev and Haswell, 2012), while OSCAs rather Ca 2+ (Yuan et al, 2014, Murthy et al, 2018, Thor et al, 2020. To trigger excitation in the flytrap cells have to be depolarized by 20-40 mV from the resting state (Hedrich and Fukushima, 2021). Thus, together MSL10 and OSCA(s) likely give rise to depolarization and Ca 2+ influx for activation of anion channels.…”