Social networking in crop plants: Wired and wireless cross-plant communications

Abstract

The plant-associated microbial community (microbiome) has an important role in plant-plant communications. Plants decipher their complex habitat situations by sensing the environmental stimuli and molecular patterns and associated with microbes, herbivores and dangers. Perception of these cues generates inter/intracellular signals that induce modifications of plant metabolism and physiology. Signals can also be transferred between plants via different mechanisms, which we classify as wired- and wireless communications. Wired communications involve direct signal transfers between plants mediated by mycorrhizal hyphae and parasitic plant stems. Wireless communications involve plant volatile emissions and root exudates elicited by microbes/insects, which enable inter-plant signalling without physical contact. These producer-plant signals induce microbiome adaptation in receiver plants via facilitative or competitive mechanisms. Receiver plants eavesdrop to anticipate responses to improve fitness against stresses. An emerging body of information in plant-plant communication can be leveraged to improve integrated crop management under field conditions.

Keywords: dodder; herbivore-induced plant volatiles; holobiont; microbe-induced plant volatiles; microbiome adaptation; mycorrhiza.

FIGURE 1

Wired and wireless phytobiome communication. Clonal plants (right) communicate via physical connections (e.g. stolons and rhizomes) or VOCs. Plants also communicate via dodder and mycorrhiza (left). Receiver plants can act as nodes to transfer defence signals against pests and pathogens to neighbouring conspecific and heterospecific plants. Volatiles and root exudates received by neighbouring plants modulate receiver plant defence systems, attract parasitoids and entemopathogens and induce plant microbiome remodelling to protect plants against imminent stress conditions [Colour figure can be viewed at wileyonlinelibrary.com]

FIGURE 2

Signals from neighbouring plants modulate signalling pathways in receiver plants and induce microbiome remodelling. Signals can be sensed by receiver proteins (e.g. ETR1 sensor for ethylene) or converted to active signals [e.g. SABP2 for salicylic acid (SA)]. Signals are transmitted through well‐characterized downstream pathways that may cross‐talk with each other. These signalling pathways regulate defence mechanisms against different groups of attackers and induce plant microbiome remodelling by changing root exudation, thereby adapting the plant holobiome to respond to imminent threats. ALMT1, aluminium‐activated malate transporter; AUX1/LAX, auxin resistant 1/LIKE AUX1; CDPK, Ca²⁺‐dependent protein kinases; CIPK, calcineurin B like proteins (CBL)‐interacting protein kinase; CTR1, constitutive triple response 1; EIN2, ethylene insensitive 2; ETR1, ethylene response 1; FIT1, FE‐deficiency‐inducing transcription factor 1; FRO2, ferric reductase oxidase 2; G3P, glycerol‐3‐phosphate; IAA, indole‐3‐acetic acid; IRT1, iron‐regulated transporter 1; JAZ, Jasmonate Zim domain protein; Med25, mediator 25; MeJA, methyl jasmonate; MeSA, methyl salicylate; NPR, non‐expresser of PR genes; ORA59, octadecanoid‐responsive Arabidopsis 59; SABP2, SA‐binding proteins 2; SCFCOI1, Skp1‐Cul1‐F‐box protein coronatine insensitive 1 [Colour figure can be viewed at wileyonlinelibrary.com]

FIGURE 3

Illustration of the signal input‐transfer‐output model in plant–plant communication. Molecular patterns, volatiles and effector proteins of pests and pathogens elicit plant signalling pathways that promote volatiles emission and root exudation. Plant signals can be delivered to neighbouring plants through the atmosphere or soil (wireless communication), or transferred through mycorrhiza, fungi and odder (wired communication). Signals can be converted to their active form by receiver plant proteins. Signal perception by neighbour plants activates signalling pathways and phosphorylation cascades, which subsequently induce the expression of defence‐related proteins and metabolites. Signal perception also changes the root exudate and recruits beneficial microbes. BZ, benzoxazinoid; GLVs, green leaf volatiles; HAMPs, herbivore‐associated molecular patterns; JA, jasmonic acid; MAMPs, microbe‐associated molecular patterns; MAPKs, mitogen‐activated protein kinases; MEP, methylerythritol phosphate; MeSA, methyl salicylate; MVA, mevalonic acid; SA, salicylic acid; TFs, transcription factors; VOCs, volatile organic compounds [Colour figure can be viewed at wileyonlinelibrary.com]