ENGINEERING PLANT-MICROBE INTERACTION FOR NEXT GENERATION
AGRICULTURE
The one health concept is based on a growing understanding that humans,
animals, plants, microbiomes, and the environment are inseparably linked
and impact each other constantly. The presence and stress levels
experienced by different organisms within an ecosystem could therefore
be transmitted from one to another through cell-to-cell ROS wave
signaling. Stress experiences may be transmitted between plants and the
soil microbiomes, by variations in the exchange of ROS signals. The
application of genetic engineering approaches that serve to support
symbiosis by blocking or minimizing the recognition-induced oxidative
burst and activating host defenses must take such interactions into
account, not only because they could increase the susceptibility of
plants to pathogen attack but because they could also disrupt or
interfere with a wide range of inter-organism communications within a
given ecosystem.
Next-generation agriculture will be comprised of at least three
components: enhanced crop production, minimal agri-inputs in the form of
pesticides/fertilizers, and enhanced microbial carbon sequestration
(Fig. 4A). Although, tailored plant-microbe interactions promise to meet
all these three expectations, the AKP (Anna Karenina Principle) must be
addressed. AKP considers that dysbiotic microbiomes are intrinsically
different, while healthy microbiota are similar (Arnault, Mony, &
Vandenkoornhuyse, 2023). Nevertheless, some strategies have already
proved to be successful. For example, rhizosphere microbiome
transplantation (RMT), in which microbial communities from either
extreme environments or from a tolerant cultivar are inoculated to
enhance growth or suppress stress responses (Fig. 4B) (Poppeliers,
Sanchez-Gil, & de Jonge, 2023). RMT-mediated enhanced plant growth is
poorly understood but could be stress-specific in nature. For example,
changes in the drought and cold tolerance of tree species were
associated with increased and decreased AMF diversity, respectively
(Allsup et al., 2023).
Manipulation of the soil microbiome, associated crop management
practices, and applied crop design are important components of solutions
to address climate change. Much attention has also focussed on
engineering nitrogen-fixing nodulation traits in non-leguminous crop
plants (Huisman & Geurts, 2020). However, environmental perturbations
exert effects on the diversity of plant microbial communities, with
varying effects depending on the plant species and developmental stage.
For example, drought increases the release of flavonoids in root
exudates. These reshape the root microbiome by attractingAeromonas species that enhance dehydration resistance in plants
(He et al., 2022). In addition, core bacterial commensals and host
tryptophan-derived specialized metabolites participate in the control of
fungal species (Wolinska et al., 2021). The changes in the relative
abundance of Actinobacteria and Proteobacteria were reported in rice
cultivated under drought conditions, an effect that persisted after
stress alleviation (Santos-Medellin et al., 2021). In sorghum, drought
increased the abundance of Actinobacteria and decreased
pathogenic genera (Fusarium, Gibberella, and Sarocladium )
compared with well-watered controls (Gao et al., 2020; Xu et al., 2018).
Drought-stressed sorghum plants in soils with Arthrobacterbacteria suffered more than those in which bacteria of the genusVariovorax were abundant (Qi et al., 2022). In contrast,Arthrobacter alleviated drought-stress effects in wheat (Hone et
al., 2021). The presence of endospheric Streptomyces was
correlated with drought tolerance in several plant species (Fitzpatrick
et al., 2018).
Microbiome-inspired methods are promising innovations to enhance the
stress resilience of crops. Roots grown in natural- and agro-ecosystems
preferentially recruit PBB and AMF in drought situations (Song & Haney,
2021; Williams & de Vries, 2020; Zhao et al., 2023). Therefore,
commercial AMF inoculants, added as a supplement to agricultural lands,
have considerable potential in the alleviation of drought and nutrient
deficiency in plants (Salomon et al., 2022). The application of
microbial consortia may be more efficient than single-strain inocula in
enhancing stress tolerance (Bradáčová et al., 2019). However, while AMF
richness increases in barley roots under drought, AMF performance
(colonization and the abundance of arbuscules and vesicles) decreases,
indicating antagonistic interactions (Sendek et al., 2019). However,
while drought increases the prevalence of beneficial microbes in
rhizosheaths, it also increases the risk of penetration by harmful fungi
(Lei et al., 2023). Moreover, a limitation factor in the application of
such information concerns the diverse nature of AMF functionality
depending on environmental effects.
Native synthetic microbial communities (SynComs) from plants grown under
optimal conditions can be used to boost plant growth in poor soils (Fig.
4C) (M. Jiang et al., 2023). For example, SynComs application promotes
the growth of A. thaliana , in an innate immunity-dependent manner
(Wolinska et al., 2021). Cross-kingdom (fungi and bacteria) SynComs were
more effective in suppressing fusarium-wilt disease in tomato than fungi
or bacteria alone (X. Zhou et al., 2022). RMT and SynComs have yet to be
tested for field applications, due to low efficiency in isolating
functionally beneficial microbiomes. Multiple approaches based on
screening natural variation, mathematical modeling, RAMAN-spectra, and
successive passaging are being used to map the microbial community
networks (Chen et al., 2021; X. He et al., 2021; Morella et al., 2020).
The root-secreted chemicals or exudates comprised of photosynthetically
fixed carbon as well as diverse signaling molecules including
γ-aminobutyric acid, malate, and citrate, also contribute to shaping
rhizosphere microbiome (Fig. 4D) (W. Zhang & Mason, 2022).In addition,
microbe-derived secretory proteins YukE cause iron leakage in plant
roots, which contributes to root colonization by beneficial
rhizobacterium Bacillus velezensis (Y. Liu et al., 2023).
Microbiome engineering to improve the composition of root
exudates/secretomes will help determine the host-derived factors that
synchronize interactions between beneficial and resident microbiomes
(Escudero-Martinez & Bulgarelli, 2023). QTLs that determine the
root-microbiota composition of crops contain genes such as the iron
regulator FIT and water channel aquaporin SlTIP2.3 in tomato (Oyserman
et al., 2022) and Nucleotide-Binding-Leucine-Rich-Repeat (NLR) in barley
(Escudero-Martinez et al., 2022). Apart from the genotypes, the
heritable component also needs to be accounted, especially in the
context of microbiome-assisted molecular crop breeding.