Plants under pressure: activation of stress hormones

Plants Get Stressed Too (even more in an ever-changing environment)

Throughout their lives, plants are exposed to a wide range of environmental challenges that can affect their growth and jeopardize their health. These external threats can be categorized as abiotic stresses if caused by “non-living factors” (e.g., freezing/chilling or heat, water deficit or flooding, UV radiation, soil salinity, nutrient deficiency, air pollution and soil contamination) or as biotic stresses if caused by “living factor” (e.g., viruses, bacteria, fungi, nematodes, insects, weeds).

Depending on the intensity and duration of the stress, environmental factors can mildly affect the development of plant organs (below and/or above ground) or seriously impact plant reproduction. In the worst-case scenario, plants can experience a combination of environmental stressors that greatly threatens their survival.

Stressed Organs Send Signals Outside and Inside the Plants

In March 2023, the scientific journal Cell published a research article that showed a curious response of plants under pressure: they are “calm” when grown in optimal conditions but “scream” when stressed. The science news has gone around the world and these unexpected findings went viral on social media. What does the article exactly show?

The research team coordinated by Prof Lilach Hadany (School of Plant Sciences and Food Security, Tel Aviv University) found that tomato and tobacco plants start emitting ultrasonic sounds in the nearby (3-5 metres away) two days after suffering water deprivation or physical damage. This phenomenon could be caused by cavitation – the generation of air bubbles when water columns break down in plant stems subjected to drought or wounding. Human beings are not able to hear these frequencies, but scientists are currently investigating the possibility that other organisms – such as insects, small mammals, other plants – living in the same environment can perceive the sounds and react.

Besides “cries of pain”, stressed plants also experience internal hormonal fluctuations, like animals. In fact, it has long been established that plants living in suboptimal conditions accumulate stress hormones that act within the plant body to trigger a wide array of defensive and adaptive responses at the molecular, cellular, and physiological levels.

Hormones and Phytohormones

Multicellular organisms (such as animals, plants, and fungi) produce signalling molecules called hormones that move through their bodies to regulate developmental and physiological processes. These chemical messengers are active at very low concentrations and can travel from their site of production to distant tissues and organs, where they provoke molecular and cellular responses.  

The term phytohormones was coined by Frits Went and Kenneth Thimann in 1937 to describe organic compounds that can act locally and systemically as plant growth regulators. Phytohormones are generally required to regulate the formation of different organs throughout the plant life cycle, but some of them (e.g., Abscissic Acid and Jasmonic Acid) – are also activated in stress conditions to coordinate plant growth and defence, often inhibiting developmental processes to increase survival.

Jasmonates: Production, Transport & Signal Transduction

This class of lipid-derived phytohormones was first described in 1962 and named Jasmonates (JAs) as their structure was identified from oil extracts of Jasminum grandiflorum flowers. Since their discovery, several research groups worldwide have been investigating the metabolic pathways that contribute to the biosynthesis of JAs and accumulation of their precursors, as well as catabolic reactions that transform bioactive hormones into inactive compounds (nicely reviewed by Wasternack & Hause, 2013 and Wasternack & Song, 2017).

JAs derive from polyunsaturated fatty acids, such as α-linolenic acid, through a complex series of metabolic reactions that take place sequentially in different compartments of the plant cell (e.g., chloroplast, peroxisome, cytosol). Some JAs precursors are also stored in the vacuole.

How can the stress induce the production of JAs? Upon external attack, damaged plants can detect “foreign metabolites” – such as Microbe-Associated Molecular Patterns (MAMPs) and Pathogen-Associated Molecular Patterns (PAMPs) – that act as elicitors, molecules able to trigger a cascade of cellular and molecular events (signal transduction pathway) leading to the induction of JA metabolism.

Accumulated JAs can be transported locally (short distance transmission to neighbouring cells) or systemically (long distance transmission to distant cells through vasculatures). For example, phloem-mediated transport is essential for leaf-to-leaf and stem-to-stem communications. Local and systemic signalling is facilitated by a family of JAs transporter (named JAT) with different subcellular localizations, which promote hormone cellular import/export and nuclear import (reviewed by Li et al., 2021). 

Downstream Effects of the JA Pathway: Defence Response to Pathogen Attack

In the nucleus, JAs trigger changes in the transcription of selected genes that are involved in stress signalling and defence response. For example, the accumulation of JAs in response to insect attack activates the expression of genes that encode proteins with toxic effects or volatile organic compounds (VOCs) that attract natural enemies of the herbivores (reviewed by Erb & Reymond, 2019). Likewise, a derivative of JA induces the biosynthesis of terpene, a secondary metabolite with a strong antifungal activity that confers resistance to grey mould caused by the necrotrophic pathogen Botrytis cinerea in strawberry (reported in Zhang et al., 2022).

Curiosity: JAs & Evolution of Plant Carnivory

JAs are also involved in the interaction between insects and carnivorous plants living in nutrient-poor environments. Precisely, the JA pathway is activated upon the second mechanical stimulus in the plant Dionaea muscipula (commonly known as Venus flytraps), followed by the induction of genes encoding hydrolases – lytic enzymes used in the digestion of insect preys trapped in the plant lobes.

Suggested Reading

Abiotic stress responses in plants | Nature Reviews Genetics

Sounds emitted by plants under stress are airborne and informative: Cell

Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany | Annals of Botany | Oxford Academic (oup.com)

Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription | Journal of Experimental Botany | Oxford Academic (oup.com)

Metabolism, signaling, and transport of jasmonates – ScienceDirect

Arabidopsis Basic Helix-Loop-Helix Transcription Factors MYC2, MYC3, and MYC4 Regulate Glucosinolate Biosynthesis, Insect Performance, and Feeding Behavior | The Plant Cell | Oxford Academic (oup.com)

Molecular Interactions Between Plants and Insect Herbivores | Annual Review of Plant Biology (annualreviews.org)

Jasmonate increases terpene synthase expression, leading to strawberry resistance to Botrytis cinerea infection | SpringerLink

The Venus Flytrap Dionaea muscipula Counts Prey-Induced Action Potentials to Induce Sodium Uptake: Current Biology (cell.com)

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