3.3  Wireless signal output: Receiver plant response to biotic/abiotic stresses
The transferred signal is perceived by neighboring (receiver) plants and augments biotic/abiotic stress resistance responses. VOC-mediated plant stress responses have been demonstrated in numerous studies, although the ethylene receptor ETR1 is the only plant VOC receptor identified to date (Chang, Kwok, Bleecker & Meyerowitz, 1993). Future research may discover additional receptors to plant volatile organic compounds (VOCs).
Recent studies identified different mechanisms whereby receiver plants perceive VOCs from neighbor plants. VOCs can be absorbed by a wax layer on the epidermal cell, which traps VOCs and slowly releases them to attract or repel herbivores and their parasitoids and entomopathogens (Camacho-Coronel, Molina-Torres & Heil, 2020, Lin, Hussain, Avery, Qasim, Fang & Wang, 2016).
Some trapped volatiles such as methyl salicylate (MeSA), MeJA, and indole can be converted to the active plant hormones SA, JA, and indole-3-acetic acid (IAA), respectively (Figure 2,3) (Bailly, Groenhagen, Schulz, Geisler, Eberl & Weisskopf, 2014, Rivas-San Vicente & Plasencia, 2011). Some enzymes metabolize trapped volatiles such as (Z )-3-hexenol to the more active derivative (Z )-3-hexenylvicianoside (Sugimoto, Matsui, Iijima, Akakabe, Muramoto, Ozawa, Uefune, Sasaki, Alamgir & Akitake, 2014). Some GLVs induce plasma membrane potential depolarization in receiver plants, thereby activating reactive oxygen species (ROS) and calcium signaling (Figure 2) (Zebelo, Matsui, Ozawa & Maffei, 2012).
The perception of VOCs modifies the transcriptome, proteome, and metabolome in receiver plants (Kwon, Ryu, Lee, Park, Han, Lee, Lee, Chung, Jeong, Kim & Bae, 2010, van Dam & Bouwmeester, 2016, Zhang, Kim, Krishnamachari, Payton, Sun, Grimson, Farag, Ryu, Allen, Melo & Pare, 2007). In some cases, VOCs do not significantly change gene expression profiles and metabolic activity, but prime the plant to respond more rapidly and robustly to upcoming threats (Paschold, Halitschke & Baldwin, 2006, Quintana-Rodriguez et al. , 2015). Plant volatile (Z )‐3‐hexenyl acetate directly induces JA- and abscisic acid–related gene expression, whereas indole primes these genes in maize against Spodoptera littoralis (Hu, Ye & Erb, 2019). Several studies report that primed plants activate defense-related pathways based on the attacker identity rather than the inducer (Moreira, Nell, Katsanis, Rasmann & Mooney, 2018, Sharifi & Ryu, 2017). For example, VOCs from plants infested with general or specialized herbivores activate similar defense pathways and VOC emission profiles in healthy neighbors. By contrast, primed receiver plants mount a specific set of defense mechanisms based on the type of attacker (Moreira et al. , 2018).
Infochemicals from neighbor plants can activate master regulatory systems involved in plant innate immunity, including leucine-rich repeat-receptor-like kinase, mitogen-activated protein kinases, WRKY transcription factors, and systemic acquired resistance (Figure 2, 3) (Dombrowski, Kronmiller, Hollenbeck, Rhodes, Henning & Martin, 2019, Dombrowski & Martin, 2018, Lee, Kim, Lee, Ahn & Ryu, 2020, Mirabella, Rauwerda, Allmann, Scala, Spyropoulou, Vries, Boersma, Breit, Haring & Schuurink, 2015, Wenig et al. , 2019, Ye, Glauser, Lou, Erb & Hu, 2019). D-Lactic acid secreted by the microalga Chlorella fuscaprimed defense in Arabidopsis thaliana against Pseudomonas syringae pv. tomato DC3000 by increasing the expression of WRKY transcription factors and cysteine-rich receptor-like kinases, and induced both SA- and JA-dependent pathways (Lee et al. , 2020).
In inter-plant communication, volatile organic compounds (VOCs) modulate receiver plant physiology and directly or indirectly affect other plant holobiome members. VOCs captured by receiver plant wax display fungicidal and bactericidal activity for several days (Camacho-Coronelet al. , 2020). GLVs and terpenoid volatiles have strong fungicidal and bactericidal activity in vitro and in planta (Huang, Sanchez-Moreiras, Abel, Sohrabi, Lee, Gershenzon & Tholl, 2012, Pontin, Bottini, Burba & Piccoli, 2015, Quintana-Rodriguezet al. , 2015). VOCs can alter parasitoid attraction and entomopathogenic fungi performance in both donor and receiver plants (Desurmont, Xu & Turlings, 2016, Lin et al. , 2016, Xu, Desurmont, Degen, Zhou, Laplanche, Henryk & Turlings, 2016). VOC emission in aboveground and below-ground parts may attract or repel herbivores and plant pathogenic nematodes (Ali, Alborn & Stelinski, 2011, D’Alessandro, Erb, Ton, Brandenburg, Karlen, Zopfi & Turlings, 2014, Rasmann, Kollner, Degenhardt, Hiltpold, Toepfer, Kuhlmann, Gershenzon & Turlings, 2005).
Root exudates act as critical triggers to activate resistance in neighboring plants by diffusing through the soil to neighboring roots. Root exudates such as SA transfer the SAR signal to neighboring plants and synchronize their microbiomes (Kong, Song, Sim & Ryu, 2020, Orlovskis & Reymond, 2020, Song et al. , 2016). Plants exploit microbiome adaptation to facilitate conspecific survival according to kin selection theory, or to compete for heterospecificity. Airborne signals from wound-damaged plants regulated the ALMT1 transporter in receiver Arabidopsis plants to release malic acid into the rhizosphere (Figure 3). Malic acid recruits B. subtilis to colonize Arabidopsis roots and induce systemic resistance to different stresses (Rudrappa, Czymmek, Pare & Bais, 2008, Sweeney, Lakshmanan & Bais, 2017).
A (–)-loliolide root exudate at a physiological concentration of 5 nmol g−1 soil induces the release of the benzoxazinoid compound 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) exudate from wheat roots (Kong et al. , 2018b). DIMBOA is a putative allelochemical with several other roles in the rhizosphere. DIMBOA regulates the root metabolome and exudation, which have important roles in shaping the root microbiome (Cotton et al. , 2019, Kudjordjie, Sapkota, Steffensen, Fomsgaard & Nicolaisen, 2019). DIMBOA-treated plants recruit specific bacterial families and species such asPseudomonas putida , thereby increasing plant resistance to several stresses (Neal & Ton, 2013). P. fluorescens increases DIMBOA and primed resistance against the fungal pathogenSetosphaeria turcica in maize (Zhou, Ma, Lu, Zhu & Yan, 2020). The populations of bacterial plant pathogens such as Xanthomonadaceae and Agrobacterium tumefaciens decreased in benzoxazinoid-treated plants (Cotton et al. , 2019, Kudjordjie et al. , 2019).
Any change in cumarin, sesquiterpenes, and diadzein by airborne signals and root exudates will change plant microbiomes (Chen, Jiang, Liu, Liu, Zhao, Liu, Gan, Hallab, Wang, He, Ma, Zhang, Jin, Schranz, Wang, Bai & Wang, 2019b, Okutani, Hamamoto, Aoki, Nakayasu, Nihei, Nishimura, Yazaki & Sugiyama, 2020, Stringlis, Proietti, Hickman, Van Verk, Zamioudis & Pieterse, 2018). Activation of defense hormones (e.g., JA and SA) by airborne signals (e.g., MeSA, 3-pentanol, or effectors of aphid/whitefly pest) induces microbiome adaptation in plants (Lee, Lee & Ryu, 2012, Mannaa et al. , 2020, Song, Choi & Ryu, 2015, Yang, Yi, Kim, Lee, Lee, Ghim & Ryu, 2011). Microbiome adaptation in these examples reduces disease severity caused by several plant pathogens and pests, probably by recruiting beneficial bacteria such as B. subtilis (Leeet al. , 2012, Song et al. , 2015). The rhizosphere microbiome also modulates root metabolism and exudation by azelaic acid as a potential signal molecule (Figure 3) (Korenblum, Dong, Szymanski, Panda, Jozwiak, Massalha, Meir, Rogachev & Aharoni, 2020). Activation of the two JA pathway branches differentially shape the root microbiome. The Arabidopsis mutants myc2 and med25 alter root exudate (Figure 3). Similar changes in some categories of root exudate were observed in mutants of both branches, but some root exudates were differentially synthesized. Clostridiales were abundant but declined in mutants of both branches. Bacillus , Lysinibacillus , andStreptomyces populations increased in the med25 mutant, whereas the Enterobacteriaceae population increased in the myc2mutant (Carvalhais et al. , 2015). Med25 has an important role in regulating density recognition in Arabidopsis and changing root architecture by increasing root response to auxin (Munoz-Parra, Pelagio-Flores, Raya-Gonzalez, Salmeron-Barrera, Ruiz-Herrera, Valencia-Cantero & Lopez-Bucio, 2017).