Bryophytes can recognize their neighbours through volatile organic compounds

Abstract

communication between vascular plants through volatile organic compounds (Vocs) impacts on ecosystem functioning. However, nothing is known about that between non-vascular plants. To investigate plant-plant Vocs interaction in bryophytes we exposed rare peatland moss Hamatocaulis vernicosus to Vocs of its common competitor Sphagnum flexuosum in an air-flow system of connected containers under artificial light, supplemented or unsupplemented by far-red (FR) light. When exposed to Vocs of S. flexuosum, shoots of H. vernicosus elongated and emitted six times higher amounts of a compound chemically related to β-cyclocitral, which is employed in stress signalling and allelopathy in vascular plants. The VOCs emission was affected similarly by FR light addition, possibly simulating competition stress. This is the first evidence of plant-plant VOCs interaction in non-vascular plants, analogous to that in vascular plants. The findings open new possibilities for understanding the language and evolution of communication in land plants. Interactions are crucial for the survival of individuals in ecological communities 1. Consequently, animals and plants perceive a variety of cues by which they can ascertain what is in the proximity. Until the end of the twentieth century, however, the active sharing of information seemed solely the domain of animals. Plants were viewed as passive, stationary organisms, with only basic interactions with other organisms 2 , apart from pollinators. With the discovery of plant communication 3,4 , it became evident that plants use light 5 , touch 6-9 , vibrations 10 and chemicals 11-13 to communicate in an intricate web of multitrophic interactions that affect functioning of ecosystems. Volatile organic compounds (VOCs) are involved in communication in eukaryotic and prokaryotic organisms including animals and vascular plants 14 , bacteria 15 , brown algae 16 , and fungi 17. These secondary metabolites with low molecular weight and high vapour pressure at ambient temperature can move freely through the air. They are produced in cytosol (organelles or cytoplasm) and are possibly transported outside the cell through lipophilic carriers (in aqueous environments of cytosol and cell wall) and ABC transporters (through lipophilic plasma membrane 18,19). The production of VOCs by plants depends on genetic identity of the individual, life history and health, plant organ, photoperiod, light quality (e.g., red to far-red (R/FR) ratio), symbiotic organisms and other factors 1,20-23. Hence, each organism has a specific VOC blend including compounds unique for the given taxon 24 as well as chemicals with specific ecological meaning (e.g. 25). Species that can detect and decipher the encoded information can use VOCs in interactions, as a source of information. Plant-plant VOC interaction often takes the form of eavesdropping. Plants can estimate the strength of their neighbouring competitors and, accordingly, adjust their growth 26. Parasitic plants can use VOCs to locate their hosts 24. VOCs could even be use...

Plant volatiles as cues and signals in plant communication

“…From an evolutionary perspective, one of the oldest plant species is the bryophytes. The first evidence of plant–plant interactions via VOCs in non‐vascular plants was observed in a study showing that bryophytes can recognise their neighbours (Vicherová, Glinwood, Hájek, Šmilauer, & Ninkovic, 2020). Upon receiving VOCs from Sphagnum flexuosum , peatland moss ( Hamatocaulis vernicosus ) altered its growth pattern and emission of β‐cyclocitral to a degree six times higher than that of the negative control.…”

“…Plants coexist in different communities wherein they unavoidably interact with neighbouring plants. Consequently, plants have adapted a variety of strategies to rapidly exchange volatile messages and mitigate the impact of complex biotic and abiotic factors from their surroundings (Douma, Vermeulen, Poelman, Dicke, & Anten, 2017; Vicherova, Glinwood, Hajek, Smilauer, & Ninkovic, 2020). One adaptation mechanism that plants have developed is the ability to produce and emit an array of different volatile organic compounds (VOCs) (Dudareva, Klempien, Muhlemann, & Kaplan, 2013), presenting a fingerprint of the plant's current physiological status.…”

Control of theAzollasymbiosis sexual reproduction: ferns to shed light on the origin of floral regulation?

“…MpPHY and MpPIF were required to mediate the response (Inoue et al, 2019). Figure 2F) that may stem from alternative cues such as volatile organic compounds released by neighbors (Vicherová et al, 2020). Taken together, results presented in this work signify that, for the first time, RD of the Azolla fern symbiosis is amenable to experimental enquiry.…”

Friends, neighbours and enemies: an overview of the communal and social biology of plants

“…This may be particularly the case in basal land plant lineages (mosses, liverworts, hornworts) which are particularly characterized by short‐range dispersal through asexual reproduction, leading to continuous assemblies of closely related individuals (Frey & Kürschner, 2011; Partridge & Harvey, 1988; Renzaglia, Joel Duff, Nickrent, & Garbary, 2000; Taylor, Kerp, & Hass, 2005). Within species, related mosses co‐operatively avoid overgrowth, (Proust et al, 2011), whereas heterospecific mosses seem to actively compete in response to light and VOC cues from neighbours (Vicherová et al, 2020). While species‐level recognition remains largely uncharacterized, it is an intriguing prospect deserving more attention.…”

“…Plants were traditionally viewed as passive, affected by their neighbours only through indirect effects on resource availability (Pierik, Mommer, & Voesenek, 2013). Until the early 1980s, there was little indication that plants might have interactions every bit as complex as those seen in animals (Vicherová, Glinwood, Hájek, Šmilauer, & Ninkovic, 2020). However, as an ever‐increasing body of work is demonstrating, plants do detect, respond to and interact with their neighbours.…”