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).