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Improving crop salt tolerance
through soil legacy effects
Yue Ma
1,2
, Chunyan Zheng
1
, Yukun Bo
1
, Chunxu Song
3,4,5
and Feng Zhu
1
*
1
Key Laboratory of Agricultural Water Resources, Hebei Key Laboratory of Soil Ecology, Center for
Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy
of Sciences, Shijiazhuang, China,
2
University of Chinese Academy of Sciences, Beijing, China,
3
State
Key Laboratory of Nutrient Use and Management, College of Resources and Environmental Sciences,
National Academy of Agriculture Green Development, China Agricultural University, Beijing, China,
4
Key Laboratory of Plant-Soil Interactions, Ministry of Education, China Agricultural University,
Beijing, China,
5
National Observation and Research Station of Agriculture Green Development,
Quzhou, China
Soil salinization poses a critical problem, adversely affecting plant development
and sustainable agriculture. Plants can produce soil legacy effects through
interactions with the soil environments. Salt tolerance of plants in saline soils is
not only determined by their own stress tolerance but is also closely related to
soil legacy effects. Creating positive soil legacy effects for crops, thereby
alleviating crop salt stress, presents a new perspective for improving soil
conditions and increasing productivity in saline farmlands. Firstly, the formation
and role of soil legacy effects in natural ecosystems are summarized. Then, the
processes by which plants and soil microbial assistance respond to salt stress are
outlined, as well as the potential soil legacy effects they may produce. Using this
as a foundation, proposed the application of salt tolerance mechanisms related
to soil legacy effects in natural ecosystems to saline farmlands production. One
aspect involves leveraging the soil legacy effects created by plants to cope with
salt stress, including the direct use of halophytes and salt-tolerant crops and the
design of cropping patterns with the specific crop functional groups. Another
aspect focuses on the utilization of soil legacy effects created synergistically by
soil microorganisms. This includes the inoculation of specific strains, functional
microbiota, entire soil which legacy with beneficial microorganisms and tolerant
substances, as well as the application of novel technologies such as direct use of
rhizosphere secretions or microbial transmission mechanisms. These
approaches capitalize on the characteristics of beneficial microorganisms to
help crops against salinity. Consequently, we concluded that by the screening
suitable salt-tolerant crops, the development rational cropping patterns, and the
inoculation of safe functional soils, positive soil legacy effects could be created to
enhance crop salt tolerance. It could also improve the practical significance of
soil legacy effects in the application of saline farmlands.
KEYWORDS
saline soil, halophytes, salt-tolerant crops, beneficial microorganism, salt tolerance
Frontiers in Plant Science frontiersin.org01
OPEN ACCESS
EDITED BY
Dinesh Yadav,
Deen Dayal Upadhyay Gorakhpur University,
India
REVIEWED BY
Yuri Shavrukov,
Flinders University, Australia
Abhishek Joshi,
Mohanlal Sukhadia University, India
*CORRESPONDENCE
Feng Zhu
zhufeng@sjziam.ac.cn
RECEIVED 06 March 2024
ACCEPTED 22 April 2024
PUBLISHED 10 May 2024
CITATION
Ma Y, Zheng C, Bo Y, Song C and Zhu F
(2024) Improving crop salt tolerance
through soil legacy effects.
Front. Plant Sci. 15:1396754.
doi: 10.3389/fpls.2024.1396754
COPYRIGHT
© 2024 Ma, Zheng, Bo, Song and Zhu. This is
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terms of the Creative Commons Attribution
License (CC BY). The use, distribution or
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copyright owner(s) are credited and that the
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is permitted which does not comply with
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TYPE Review
PUBLISHED 10 May 2024
DOI 10.3389/fpls.2024.1396754
1 Introduction
In recent years, land degradation caused by climate change has
posed a huge challenge to agricultural production. In the absence of
major technological breakthroughs in agriculture, existing arable
land resources are hardly sufficient to support global food security
(German et al., 2017;Hartmann and Six, 2023). Saline farmland is
an important reserve resource of arable land with great potential for
ensuring food security and sustainable agricultural development
(Negacz et al., 2022). Therefore, finding solutions to increase the
productivity of saline farmland and improve crop tolerance to saline
stress has become an important research topic currently (Munns
and Tester, 2008).
Soil salinization is a global environmental problem, with more
than 833 million hectares of soil and more than 10% of farmland
affected by salinization (FAO, 2021), causing at least 25% of crops to
suffer from varying degrees of yield loss due to persistent salt stress,
with a serious impact on food security (Farooq et al., 2017;Kumar
et al., 2022). Soil salinization leads to reduced crop yield because the
significant negative impacts on seed germination by disrupting the
membrane permeability of the seed embryo and increasing the
osmotic stress on seeds (Deng et al., 2014). For salt-sensitive crops,
seed germination rate, germination time, and the length of the
plumule are all affected by salt stress (Abbas et al., 2012). Persistent
salt stress during the crop growth phase leads to crop water loss and
ion toxicity due to increased cellular osmotic pressure and
disruption of cell membranes (Läuchli and Grattan, 2007). Salt
stress also reduces nutrient uptake by inhibiting crop root growth
(Burssens et al., 2000;West et al., 2004), inhibits photosynthesis by
decreasing the crop’s leaf area (Hu et al., 2022), and ultimately
affects crop yield and quality.
Moreover, the survival of microorganisms is directly associated
with plant and soil environments (Pulleman et al., 2012). Salt stress
can reduce the abundance and activity of soil microbial
communities (Rietz and Haynes, 2003), affecting the composition
of functional soil microbes (Zhang et al., 2019), and disrupting the
stability of microbial networks (Li et al., 2023a). This disruption
affects nutrient cycling (Bai et al., 2012) and material utilization
(Elmajdoub and Marschner, 2013) ultimately affecting the
ecological functions of soil microbial communities (Zhang et al.,
2023). Weakened ecological functions of microbial community, in
turn, affect plant-microbe interactions (Etesami and Beattie, 2017),
as manifested by reduced microbial colonization (Li et al., 2023a)
and impaired plant growth (Jansson et al., 2023).
Both plants and soil microorganisms have developed specific
abilities and mutualistic associations to cope with various stresses
(Zhao et al., 2020;Liu et al., 2022). Halophytes and salt-tolerant
plants, as the dominant vegetation in saline environments, are better
adapted to saline stresses and have formed unique strategies
improving their adaptability through such pathways as salt gland
excretion (Yuan F. et al., 2016), ionic and osmotic regulation
(Zhu, 2016), antioxidant defenses (Apse and Blumwald, 2002)and
root structural modifications (Yu et al., 2022). Soil microorganisms
also have various salt-tolerance strategies, such as salt accumulation
and synthesis of organic osmotic material to adapt to high-salt
environments (Gunde-Cimerman et al., 2018). Meanwhile,
beneficial microorganisms can influence performance of their host
plants under harsh conditions (Wang and Song, 2022). For example,
arbuscular mycorrhizal fungi can help host plants to cope with abiotic
stresses like drought, salt, etc., by improving plant water utilization,
regulating photosynthesis and maintaining osmotic balance (Borde
et al., 2017).
In addition, soil legacy effects are microbiological and
functional substance traits retained in the soil by the plants,
which influence the growth of succeeding plants (Van der Putten
et al., 2013). The formation of soil legacy effects is the process of
plant-microbe interactions in which plants respond to stressful
stimuli and mobilize the required metabolites and functional
microorganisms, thus promoting the growth of their own and
succeeding plants as well as increasing their tolerance (Bakker
et al., 2018). So, the application of soil legacy effects may also
help to refine the way we cultivate and manage crops for agricultural
production (Mariotte et al., 2018;Carrion et al., 2019;Cordovez
et al., 2019). Therefore, based on the theoretical foundation of soil
legacy effects in natural ecosystems, it is important to further
explore the mechanism of crop-soil-microbe interactions in saline
farmlands, which has profound implication for mitigating crop salt
stress, increasing crop productivity and improving the environment
of saline farmlands (Vukicevich et al., 2016).
2 Formation and role of soil legacy
effects in natural ecosystems
In natural ecosystems, plants and soil organisms have various
effects to soil legacy (Wardle et al., 2004;Faucon et al., 2017). Plant
species with different root structures, growth habits and ways of
interacting with soil organisms have important impacts on soil
legacy effects (Oliver et al., 2021), while plant species composition
and diversity also significantly modify such effects at the
community level (Kowalchuk et al., 2002;Lange et al., 2015). Soil
organisms, playing important roles in soil ecosystems, influence soil
legacy effects by affecting soil organic matter decomposition,
nutrient cycling and soil structure (Bardgett and Wardle, 2010).
Therefore, natural ecosystems have become a ‘database’for
exploring the mechanisms of soil legacy effects in the context of a
highly diversified plants, microorganisms and soil environmental
factors. An increasing number of studies have been carried out on
the growth characteristics, resource utilization and survival
strategies of plants and microorganisms that contribute to a
better understanding about the soil legacy effects (Bezemer et al.,
2006;Cortois et al., 2016;Bezemer et al., 2018;Heinen et al., 2020).
The diversity of plant species, plant functional traits and soil
microorganisms in natural ecosystems contributes to extensive
research on species interactions and stress adaptations. The
intricate interactions between plants and soil microorganisms
play a crucial role in promoting the stabilization of soil
ecosystems (Grayston et al., 1998;Berg and Smalla, 2009;
Berendsen et al., 2012). Above- and below-ground interactions of
plants have long-term legacy effects on biotic stresses in natural
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ecosystems and can improve plant performance and resistance
by manipulating soil microbial communities (Wurst and Ohgushi,
2015;Pineda et al., 2017). For abiotic stresses, soil microorganisms
are able to implement a variety of mechanisms to fight against them
and keep soil fertility as well as plant development in good
condition (Abdul Rahman et al., 2021). For example, drought
stress-induced dominance of fungal communities can influence
succeeding plant drought adaptation by maintaining higher rates
of litter decomposition and soil respiration (Mariotte et al., 2015).
Inoculation of drought-conditioned phyllosphere and soil microbial
communities can make plants capable of coping with repeated
drought stress (Li et al., 2022).
Plant functional group is a common concept in the study of soil
legacy effects, which refers to a group of plants that respond similarly
to ecological processes and environmental changes, such as the
grasses, forbs and legumes that are frequently mentioned in the
literature (Kulmatiski et al., 2008;Cortois et al., 2016). Different plant
functional groups can create positive or negative soil legacy effects by
accumulating soil pathogens, recruiting beneficial microorganisms
and regulating interactions with insects, etc (Petermann et al., 2008;
Latz et al., 2012;Heinen et al., 2019). Such soil legacy effects, mediated
by aboveground plant functional groups and soil microorganisms,
play a role for succeeding plant growth in terms of soil physical
properties, soil nutrient availability, soil microbial community
structure, stress tolerance and competitive coexistence relationships
(Byun et al., 2013;Strecker et al., 2015;Fischer et al., 2018;Mackie
et al., 2018;Adomako and Yu, 2023).
Different plant functional groups play distinct roles in shaping
soil legacy effects. For instance, grasses may improve soil physical
structure and water retention through dense root systems (Hanamant
et al., 2022), while legumes retain soil nutrients through nitrogen
fixation (Spehn et al., 2002). The soil legacy effects resulting from
these changes in the soil environment create more favorable
conditions for succeeding plant growth. Simultaneously, the
interaction between various plant functional groups and soil
microorganisms yields diverse soil legacy effects. Grasses and forbs
secrete different carbon compounds into the soil, recruiting different
soil microorganisms (Philippot et al., 2013). For example, the
presence of the grasses Lolium perenne not only increased the
density of active bacteria in the soil but also elevated the expression
of biocontrol genes associated with these bacteria, thereby
contributing to the productivity of succeeding plant communities
(Latz et al., 2015). Moreover, grasses positively influence other plant
functional groups by altering soil microbial communities and soil
nutrients (Cortois et al., 2016). Forbs, however, with more
decomposers and higher concentrations of chemicals in their litter,
may negatively impact succeeding plants (Bonanomi et al., 2006).
To foster positive soil legacy effects, it is essential to manage
specific plant functional groups, regulate appropriate levels of
beneficial microorganisms, decomposers and pathogenic
microorganisms, and develop diverse plant-microbe community
interactions (Carrion et al., 2019;De la Fuente Cantoet al., 2020;
Xiong et al., 2020;Song et al., 2021). However, there is a current lack
of studies exploring the application of the principle of soil legacy
effects in understanding plant salt tolerance. Most studies have
focused on the mechanism of plant’s intrinsic salt tolerance and the
utilization of specific microorganisms to enhance salt tolerance in
laboratory and simulation experiments (Li et al., 2020a;Li et al.,
2020b;Li et al., 2021a;Schmitz et al., 2022). Therefore, it is
important to address how the rules of soil legacy effects can be
developed and applied in saline farmlands.
3 Processes of plant response to
salt stress
Plants have various strategies to cope with salt stress, involving
refinement in their cellular physiology, phenotypic structures,
osmoregulation, antioxidant production, and the regulation of
signaling pathways (Van Zelm et al., 2020;Zhao et al., 2020). For
instance, plants eliminate excess salt through a salt excretion
mechanism to minimize salt-damage (Dassanayake and
Larkin, 2017). Plants can also modify their root structure, such as
developing deeper root systems to increase water uptake and mitigate
the impact of salinity (Galvan-Ampudia and Testerink, 2011). In
addition, plants respond to salt stress-induced damage by producing
antioxidants, osmotic substances and protective enzymes (Hasegawa
et al., 2000). ABA-dependent protein kinases are activated in response
to salt stress, affecting cellulose distribution, controlling root tip cells,
thus promoting salt avoidance in plant (Yu et al., 2022). Plant roots also
secrete peptides that are transferred to the leaves to induce ABA
accumulation, thereby driving stomatal closure to prevent leaf
(Takahashi et al., 2018;Yu et al., 2020). Therefore, the combined
application of these strategies enables plants to better adapt and survive
in high-salt environments.
Besides plant innate responses, the complex microbial
communities in rhizosphere soil play a critical role in host
performance and tolerance to stresses (Duranetal.,2018;Carrion
et al., 2019). These microbial communities help plants adapt to harsh
conditions by forming mutualistic relationships, participating in
nutrient uptake, producing beneficial compounds, and inducing
immune responses that support plants against stress (Hou et al., 2021).
In terms of salinity tolerance, microorganisms establish mutually
beneficial symbiotic relationships with plants through various
mechanisms, assisting them in adapting to high salt environments.
Rhizosphere microorganisms can secrete specific compounds, such as
bacterial exopolysaccharides (EPS), which improve plant ion balance,
promote soil aggregation, and thus maintain plant growth in high-salt
(Morcillo and Manzanera, 2021). Arbuscular mycorrhizal fungi
(AMF) enhance host plant salt tolerance by manipulating the
osmotic balance through mycelium, improving access to water and
nutrients (Hammer et al., 2011;Ruiz-Lozano et al., 2012). Moreover,
rhizosphere microorganisms also play a role in physiological
regulation and defense processes (Mishra et al., 2021). Plant growth
promoting rhizobacteria (PGPR) can stimulate root development and
enhance nutrient utilization under salt stress. For instance, the IAA-
overproducing strain Sinorhizobium meliloti has been found to
enhancive salt tolerance of alfalfa in saline soils by stimulating root
proliferation (Bianco and Defez, 2009). Under salt stress conditions,
the increase in the number and weight of root nodules in Acacia
gerrardii inoculated with Bacillus subtilis contributed to the
enhancement of nitrogen fixation by the roots, as well as uptake
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and systemic translocation of phosphorus by the plant (Hashem et al.,
2016a,Hashem et al., 2016b). AMF can activate an antioxidant
protection system, maintaining cell membrane stability by
decreasing permeability and malondialdehyde (MDA) content in
plants (Yang et al., 2014).
These complex processes converting salinity tolerance cannot be
separated from the dynamic interactions between plants and
microorganisms (Liu et al., 2022). In the context of climate change-
induced stress, introducing new microbial taxa had been shown to
improve plant survival in stressful environments, and plant tolerance
can be predicted by the climatic history of the microbial community
(Allsup et al., 2023). Building on this, plant-soil-microbe interactions
in salt-stressed environments may result in a history of stress
response for soil microbes and the soil environment, generating soil
legacy effects that aid succeeding plants in overcoming salt stress
(Figure 1;Li et al., 2021a;Jing et al., 2022).
4 Creating soil legacy effects to
improve crop salt tolerance
Farmlands vulnerable to saline stress often experience extreme
environmental conditions and undergo specificagricultural
management practices. These practices include high surface
evapotranspiration, low precipitation, elevated ambient
temperatures, and the application of chemicals, along with heavy
irrigation during production (Arora et al., 2018;Enebe and
Babalola, 2018). In contrast to natural ecosystems, the production
function of farmland directly determines its monoculture structure,
resulting in low plant diversity and nutrient use efficiency,
imbalanced dynamics between above-ground crops and below-
ground soil food webs, and altered crop defense mechanisms
(Savary et al., 2019). Crops cultivated in farmlands tend to
prioritize growth over defense compared to their wild
counterparts of the same species. This preference, combined with
the monoculture structure, increases the likelihood of negative soil
legacy effects between previous and succeeding crops (Mariotte
et al., 2018). The multiple stresses of saline farmlands challenge the
growth of crops and soil microbes, and there is a need to rethink
how to create soil legacy environments that are conducive to crop
growth, while optimizing agricultural practices and fostering
sustainable methods to enhance soil health and crop (Li et al., 2014).
4.1 The use of plants to create soil
legacy effects
The productivity constraints of saline farmlands primarily
result from the highly stressful environment directly impacting
the growth of aboveground crops. Most staple crops in agricultural
FIGURE 1
Processes of plant response to salt stress in natural ecosystems and possible soil legacy effects by plants. This figure shows, from left to right, three
different plant functional groups, legume, grass, and forb, which respond simultaneously through above-ground and below-ground parts to salt
stress. For above-ground parts of the plant, by refining cellular physiological and plant phenotypic structure, regulating signaling pathway, hormone
and metabolite and thus responding to salt stress. For below-ground parts of the plant, by maintaining ionic balance, producing different root
secretions, recruiting beneficial microorganisms and thus responding to salt stress. The response of above- and below-ground parts to salt stress
simultaneously with increasing the plant’s own acquisition of soil water and nutrients, promoting plant root proliferation, and maintaining the
osmolality of the plant as well as the rhizosphere, thus creating the positive soil legacy effects through this favourable response processes.
Ma et al. 10.3389/fpls.2024.1396754
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production, such as maize, wheat, and rice, show high sensitivity to
salinity stress. This sensitivity manifests itself in increased crop
water loss, plant and fruit wilting, reduced crop photosynthesis,
lowered carbon fixation, inhibited crop nutrient uptake, and slowed
growth (Atta et al., 2023). To overcome the production bottlenecks
in saline farmlands, it is necessary to harness biological resources
with inherent salt tolerance found in natural environments.
Additionally, establishing positive soil legacy effects through the
introduction of specific plant species and plant functional groups is
crucial (Figure 2).
4.1.1 The use of salt-tolerant biological resources
One feasible approach is to utilize the ability of halophytes and
salt-tolerant plants in the natural environment. Firstly, some
halophytes can absorb salt ions, and they are effective in reducing
surface soil salinity while fighting against the increase in ion levels in
tissue cells through leaf succulence (Song and Wang, 2015).
Halophytes also dissolve calcium in the soil through root
respiration, where calcium ions replace sodium ions in the cation-
exchange complex, and ultimately improve soil physical properties in
the plant’srootzone(Qadir et al., 2005). Desalinated soils resulting
from these processes contribute favorably to the subsequent growth
of plants. Secondly, both halophytes and salt-tolerant plants boast
robust root systems with strong penetration and water-holding
capacity, thus enhancing soil structure (Silva et al., 2016). This
improvement increases soil permeability and water retention post-
planting, with the positive effects on soil structure persisting over an
extended period (Liang and Shi, 2021). Finally, certain salt-tolerant
plants, such as the forage crop sweet sorghum, can develop salt
tolerance through hormonal signaling and secondary metabolites
(Chen et al., 2022). Notably, stress-induced plant secondary
metabolites have demonstrated legacy effects on succeeding plant
growth by manipulating the composition of soil microbiome (Hu
et al., 2018). Consequently, the utilization of halophytes and salt-
tolerant plants presents opportunities to desalinate saline farmlands,
improve soil conditions, or directly leverage the soil legacy effects
created by the metabolites they produce to enhance crop resilience
to salinity.
FIGURE 2
Effects of salt stress on crops and how to create soil legacy effects as well as improve crop salt tolerance in saline farmlands. The harmful effects of
salt stress on crops include weakening crop photosynthesis, increasing osmotic stress, reducing crop nutrient uptake, adding ionic toxicity, and
declining rhizosphere microbial diversity. By using halophytes, salt-tolerant plants, and plants of different functional groups, and developing the
cropping patterns of rotating, intercropping, and mixed cropping with crops, the interactions between above- and below-ground parts of the plants
can achieve the regulation of soil nutrients in saline farmlands, the desalination of surface soils, the secretion of salt-tolerant metabolite, and thus
regulating the balance of soil microorganisms, as well as triggering the interactions between plants and insects. The improvement of salt tolerance in
crops can also be achieved by screening for salt-tolerant microorganisms, inoculation with beneficial microbiota or entire soil inoculation. At the
same time, new cultivation techniques could be used to combine the beneficial microorganisms directly with the plants and to transmit the
tolerance. Crops with improved tolerance continue to produce salt-tolerant root secretions and to recruit beneficial microorganisms, thus creating
an effective recycle of crop salt tolerance. All of these processes can create positive soil legacy effects through beneficial interactions between the
above-ground and below-ground parts of the crop and influence succeeding crop.
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4.1.2 Introducing plant functional groups into
crop rotation systems
The soil legacy effects observed in natural ecosystems, facilitated
by specific functional groups of plants, can significantly impact
succeeding plants (Bezemer et al., 2006). This insight has inspired
the development of effective cropping patterns for saline farmlands,
especially considering that traditional monoculture patterns have
contributed to soil resource depletion and decreased farmland
productivity (Guo and Zhou, 2022). Grasses, have a solid research
base in the field of ecology, known for carbon sequestration,
nutrient cycling and improved soil stability (Franzluebbers, 2012;
Hanamant et al., 2022). As the understanding of grassland
ecosystem functioning continues to improve, forbs, representing a
large proportion of species and functional richness, have also been
recognized for their stress tolerance, indication of overgrazing, and
maintenance of insect diversity (Siebert et al., 2021). Legumes, aside
from being high-quality food and forage resources, are consistently
recognized for sequestering nutrients and increasing diversity in
cropping systems (Stagnari et al., 2017).
The crop rotation system of grasses and crops increased soil
organic matter and earthworm numbers, resulting in improved soil
structure compared to conventional crop rotations (Van Eekeren
et al., 2008). This legacy effect of the grasses’influence on soil
properties, then, increased the yield and seed nitrogen content of
succeeding crops (Christensen et al., 2009). Legumes are even more
beneficial to agricultural production by providing diverse services.
One aspect is that the nitrogen-fixing capacity of legumes can
continually increase the nitrogen yield of succeeding crops
(Fox et al., 2020). Moreover, the growth process of legumes releases
organic acids and other compounds, directly activate nutrients and
indirectly promote the activity of soil microorganisms, thus
increasing crop yields and soil fertility (Latati et al., 2016). Studies
have shown that the deposition of rhizosphere nitrogen in legumes
accounts for 70% of the total plant nitrogen (Fustec et al., 2010).
These deposited nitrogens have mechanisms for transfer to other
crops, affecting agricultural production potential. Although there are
fewer practices on the involvement of forbs in crop rotation, studies
have shown that forbs are rather less affected by changes in nutrient
conditions than grasses due to their ability to store nutrients in their
roots (Herz et al., 2017). Forbs are also important for maintaining the
diversity of arthropods in the environment and some forb
communities are more resistant to herbivores (Potts et al., 2010;
Van Coller et al., 2018). Therefore, introducing these plant functional
groups, such as grasses, forbs, and legumes, during crop rotation can
strategically change soil nutrient levels or indirectly regulate the biotic
and abiotic environment of saline farmlands.
Moreover, grasses and forbs exhibit different abiotic stress
tolerance mechanisms and growth strategies. Due to obvious
differences in growth, development and physiological structure
between grasses and forbs, applying knowledge of forbs to
improve salt tolerance in major cereal crops becomes challenging
(Tester and Bacic, 2005). Meanwhile, the ability of grasses to
accumulate salt ions in shoots and leaves may be weaker than
that of forbs due to fewer salt glands (Semenova et al., 2010). So,
although the planting of forbs like Suaeda salsa can effectively
reduce soil salinity, it is difficult to apply the mechanism of salt ion
accumulation and succulence in shoots of forbs to crops of grasses.
However, Poaceae, particularly within the functional group
of grasses, has a unique history of salt tolerance, including
major halophytic taxa identified as sources of halophytes
(Flowers et al., 1986). Compared to the forbs, grasses usually
maintain ion levels in aboveground tissues by limiting sodium
uptake, having high potassium/sodium selectivity, and efficient
potassium utilization, essential for survival under saline conditions
(Flowers and Colmer, 2008). Many wild-type grasses are naturally
tolerate to salt stress (Landi et al., 2017). For example, the study found
that its close wild relatives Tripsacum dactyloides and Zea perennis
both showed strong salt tolerance compared to maize (Li et al.,
2023b). The leaf surface of wild rice, Porteresia coarctata,canexcrete
salts, maintaining intercellular ion concentrations and lower sodium
to potassium ratios (Sengupta and Majumder, 2010). Grasses have
been reported to produce positive soil legacy effects by altering soil
microbial communities, influencing nutrient transfer, and even
triggering interactions between above-ground plants and insects
(Kos et al., 2015;Cortois et al., 2016;Schmid et al., 2021). Also, the
ionic changes that occur in grasses during salt tolerance are closely
related to their rhizosphere microorganisms (Hamdia et al., 2004;
Paul and Lade, 2014). Thus, by introducing plant functional groups
into the crop rotation system and combining their different ecological
functions and salt-tolerate characteristics, positive soil legacy effects
can be generated. This provides broader thinking for the improving
the soil environment in saline farmland and enhancing of crop
salt tolerance.
4.1.3 Introducing plant functional groups into
crop intercropping system
The combination of plant functional groups within the same
time and space can exert a significant influence on succeeding crops.
One notable example is the legume and grass forage matching
system, a typical forage mixing approach where the growth of
grasses synergistically enhances both the symbiotic nitrogen
fixation of legumes and the competitive nitrogen uptake of
grasses (De Deyn et al., 2012;Suter et al., 2015). Beyond
improving soil nutrient use efficiency, the extended growing
period of mixed legumes and grasses also helps suppress topsoil
salt accumulation, thereby enhancing soil quality (Li et al., 2021b).
While there are fewer studies on crop tillage systems and salt
tolerance, similar to forage mixes, crop intercropping can weaken the
negative impacts of saline farmland and may have legacy effects on
succeeding crops. Firstly, intercropping systems increase the
biodiversity of farmland ecosystems by direct introducing
companion plants, such as differential crops or salt-tolerant plants,
which provide services for saline farmland and the main crop (Yang
et al., 2021). The introduction of different plants diversifies the
rhizosphere environment, and the recruited microbial community
can promote nutrient cycling, salt transformation, and degradation in
the soil, thereby alleviating the damage of the saline environment to
the crops. For example, the introduction of legumes can improve
intercropping system resilience and resource use efficiency by
enhancing crop growth and tolerance to abiotic stresses through
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root distribution, vegetative cover, and nutrient activation (Chamkhi
et al., 2022). Furthermore, the intercropping of the halophyte Suaeda
salsa with maize significantly transferred more sodium ions to the
rhizosphere of Suaeda salsa, thereby reducing the salt content of the
maize rhizosphere (Wang S. et al., 2021). Regarding the rhizosphere
enrichment by intercropping systems, it was shown that legume-grass
crop intercropping (maize/faba bean) increased the abundance of
rhizobia and reduced pathogens in the soil. The soil legacy effects it
produced could be one of the reasons for the observed yield advantage
in intercropping systems (Wang et al., 2020). Particularly under salt
stress, the beneficial microorganisms recruited by the intercropping
system (sorghum/peanut) achieved increased crop tolerance by
altering the composition and content of metabolites (Shi et al.,
2023). Therefore, the potential positive soil legacy effects of salt-
tolerant forage mixtures and salt-tolerant crops of different functional
groups can help to develop efficient intercropping systems for
saline farmlands.
4.2 The use of soil microorganisms to
synergistically create soil legacy effects
The presence of soil microorganisms in natural ecosystems
depends on the soil environment, chemical signals provided by
plants and nutrient resources (Bai et al., 2022). In response to the
direct release of stress-responsive signals and compounds in plants,
the associated soil microorganisms undergo specificchanges
(Hartman and Tringe, 2019). These changes are closely related to
plants, especially alterations in rhizosphere microorganisms, and are
critical to support the growth and recovery potential of plants under
stress (Park et al., 2023). Salt-tolerant microorganisms capable of
thriving and multiplying in high-salt environments, directly aiding
plants in tolerating salt stress through their salt-tolerance
mechanisms (Sharma et al., 2015;Wang R. et al., 2021). Plants in
traditional environments, when confronted with salt stress, also
respond by directly recruiting beneficial microorganisms through
root secretions (Kumar et al., 2023). Furthermore, the mechanism by
which soil microorganisms regulate plant salt tolerance also involves
osmotic regulators, nutrients and soluble salts they provide to plants.
These pathways can indirectly influence plant hormones and
metabolism, stimulate plant growth and help plants overcome salt
stress (Glick, 2012;Shrivastava and Kumar, 2015). These actions not
only alleviate the negative effects of salinity but also establish soil
legacy effects that confer tolerance to succeeding plants (see Figure 2;
Zhalnina et al., 2018;Otlewska et al., 2020). Considering this, the
question arises: How can we apply the direct and indirect effects of
soil microorganisms on plant salt tolerance to saline farmland? What
measures can be taken to sustain these positive effects in
the farmland?
4.2.1 Direct utilization of soil microorganisms
Soil microorganisms play a crucial role in defending against saline
stress, and saline soils serve as a significant source of salt-tolerant
microorganisms (Zhang et al., 2023). Current research has successfully
isolated several culturable salt-tolerant strains. For instance, 70% of the
culturable strains of the root endophyte from the coastal perennial
grass Festuca rubra exhibit salt tolerance (Pereira et al., 2019). The
core microorganisms of the rhizosphere of Suaeda salsa have been
found to harbor genes encoding salt stress adaptation and nutrient
solubilization processes (Yuan Z. et al., 2016). Microbial inoculation is
a direct method of utilizing these specialized salt-tolerant microbial
resources, which can be applied to enhance plant salt stress adaptation
and promote growth. Studies have demonstrated that inoculation with
the salt-tolerant endophyte Sphingomonas prati significantly increases
the salt tolerance of Suaeda salsa by improving the antioxidant
enzyme system (Guo et al., 2021). Curvularia sp., isolated from
Suaeda salsa, can establish a beneficial symbiotic relationship with
poplar and promote its growth (Pan et al., 2018). Moreover, the
inoculation of salt-tolerant microorganisms has been gradually
extended to major crops, including soybean, maize, wheat, and
peanut. Its positive effect in mitigating salt stress has been
consistently verified in numerous indoor simulation experiments
(Ramadoss et al., 2013;Goswami et al., 2014;Zerrouk et al., 2016;
Khan et al., 2019;Shabaan et al., 2022).
In addition to the salt-tolerant microbial resources associated
with saline soils and halophytes, salt stress is alleviated by the
recruitment of beneficial microorganisms to the rhizosphere of
plants when they face with salt stress in normal environments
(Ilangumaran and Smith, 2017;Santoyo, 2021). For example, it has
been shown that 1-aminocyclopropane-1-carboxylate (ACC), a
stress-related amino acid in plants, can reshape the soil
microbiome, enhancing plant tolerance to salinity stress (Liu
et al., 2019). In addition, rice influences rhizosphere
microorganisms by producing metabolites such as salicin and
arbutin, enabling rhizosphere microorganisms associated salt
stress tolerance (Lian et al., 2020). Moreover, beneficial
rhizosphere microorganisms in plants can not only enhance salt-
tolerant properties but also synergistically improve plant responses
to salt stress by altering physiological growth processes, including
seed germination, morphological structure, and biomass
accumulation and partitioning (Pan et al., 2020). Regarding the
inoculation of beneficial microbial strains to help crops tolerant
salinity, studies have demonstrated that inoculation with
Pseudomonas flavescens D5 strain effectively increased the
biomass and antioxidant enzyme activities of barley, while
reducing the adverse effects of salt stress on barley (Ignatova
et al., 2022). Inoculation of candidate strains of Azotobacter has
also been found to increase the potassium-sodium ratio, polyphenol
and chlorophyll content, and decrease proline concentration in
maize, thereby alleviating salt stress in maize by integrating multiple
mechanisms (Rojas-Tapias et al., 2012).
Indeed, successful microbial inoculation often requires a
combination of strains rather than a single strain to enhance the
sustainability of its impact on (Verbruggen et al., 2012;Finkel
et al., 2017). Notably, double inoculation with Rhizobium and
Pseudomonas has been observed to elicit positive adaptive responses
in alfalfa under salt stress (Younesi et al., 2013). Similarly, dual
inoculation of plant growth-promoting bacteria with Bradyrhizobium
strains has proven more effective in enhancing salt tolerance in
soybean, reducing salt-induced ethylene production, and improving
nutrient uptake (Win et al., 2023). Further studies have found that
inoculation with species-specific microbiomes or whole-soil
Ma et al. 10.3389/fpls.2024.1396754
Frontiers in Plant Science frontiersin.org07
inoculation can assist plants in coping with various biotic and abiotic
stresses (De Vries et al., 2020;Ma et al., 2020;Trivedi et al., 2020). The
introduction of microbiomes or the whole-soil achieves more complex
ecological functions by coordinating microbial interactions (Pineda
et al., 2019;Trivedi et al., 2021), and it avoids the potential issue of
single strains struggling to survive inoculation into foreign soil
(Mallon et al., 2018). However, it is crucial to acknowledge the
possibility that introducing exotic microbial communities may
reshapefunctionswithinthenativemicrobialcommunity
(Amor et al., 2020). Recent evidence suggests that the beneficial
effects of microbial inoculation on plant growth are best explained as
changes in native microorganisms rather than direct effects on plants
(Hu et al., 2021). This underscores the importance of understanding
the intricate interactions occurring within the microbial community
and their influence on plant health and resilience.
While practical examples of microorganism inoculation for saline
farmland improvement are limited, the concept of soil legacy effects
suggests that enhancing saline farmland and crops can be achieved
through microbial-mediated processes. By inoculating salt-tolerant
microbial strains and communities of beneficial microorganisms, and
even inoculating the entire soil including most microorganisms, it
becomes possible to modulate crop responses to salt stress and
enhance salt tolerance. Concurrently, synergistic changes with the
inoculated microorganisms involve stress response-related
metabolites and alterations in the crop rhizosphere environments.
These changes encompass crop rhizosphere secretions, microbial
metabolites, and native microbial communities. Their persistent
influence on succeeding crop growth in the form of soil legacy
effects contributes to ongoing salt stress mitigation in saline
farmland. Thus, the application of microbial interventions holds
promise for sustainable improvements in saline farmland and crop
resilience (Cuddington, 2011;Trivedi et al., 2020).
4.2.2 Indirect utilization of soil microorganisms
Alongside traditional plant- and microorganism-based methods
for restoring saline farmlands, advanced modern agricultural
techniques with their high efficiency and precision have also found
application agricultural production (Varshney et al., 2011;Ahanger
et al., 2017). Research has focused on integrating and applying the
active components of rhizosphere exudates to soil microbial systems,
revealing improvements in soil physicochemical environments and
microbial communities associated with rhizosphere exudates. These
improvements are speculated to have an impact on plant growth (Shi
et al., 2011). Similar findings were observed in maize system, where a
significant increase in bacterial density and altered metabolic
potential in the maize rhizosphere after application of maize
rhizosphere exudates (Baudoin et al., 2003). In terms of enhancing
crop tolerance, research has shown that introducing the ability of
releasing volatile organic compounds (VOCs) into maize varieties
that do not release specific VOCs can reduce the threat of pests
(Degenhardt et al., 2009). This suggests that the introduction of
tolerant metabolites is not limited to rhizosphere exudates, and the
application of below-groundvolatiles, aswell as other tolerant signals,
offers additional possibilities for improving salt tolerance in crops on
saline farmlands. The advances in agricultural technology have also
inspired the exploration of beneficial root traits in wild relatives of
crops, the introduction of which may solve the problems faced by
saline farmlands (Preece and Peñuelas, 2020).
In the past decade, cultivation techniques have gradually
emerged, pointing to the unique microbiome existing in plant seeds
and how it spreads from generation to generation, aiding plants in
adapting to their environment and increasing tolerance (Gopal and
Gupta, 2016;Abdelfattah et al., 2023). In this context, delivering
endophytes to the next generation of crops and ensuring the
persistence of their tolerance has been achieved by combining
relevant beneficial microorganisms with plants (Wei and
Jousset, 2017). For example, a suspension of Paraburkholderia
phytofirmans PsJN was sprayed in plots at the flowering stage of
wheat in field experiment, and thus the maturation of its progeny
plants was accelerated by the introduction of this endophytic bacteria
into the flowers of the wheat parents (Mitter et al., 2017). The
advantage of this approach lies in the ability of seed endophytes to
avoid competition with native soil microorganisms, establishing
closer interactions with the plant early on. While there is currently
limited research related to this approach concerning salt tolerance in
progeny plants, seed endophytes have long been shown to provide
plants with tolerance against a wide range of stresses, participate in
plant adaptation mechanisms, and enhance plant competitiveness
(Samreen et al., 2021). Therefore, the use of these new bioculture
techniques and the genetic mechanisms of plant microbes offer
innovative avenues for improving saline farmland. These
approaches are closely related to plant-microbe interactions and are
centered around the concept of creating positive soil legacy effects.
Inspired by the mentioned approaches, microorganisms can be
used indirectly, such as through the recruitment of microorganisms
by plant rhizosphere exudates and intergenerational dissemination
of beneficial microorganisms, to create positive soil legacy effects in
saline farmland. However, it is acknowledged that microbial-related
methods of creating soil legacy effects are imperfect, and their
processes may introduce soil pathogens or other responsive
substances, necessitating further in-depth research to explore
safer methods of creating soil legacy effects (Jing et al., 2022).
5 Conclusion and future prospects
This paper provides a summary of the ways in which plants, in
collaboration with soil microorganisms in natural ecosystems, jointly
respond to salt stress. It suggests enhancing the salt tolerance of crops in
saline farmlands through the perspective of soil legacy effects. The focus
isonmeetingthesalttoleranceneedsofcropsbycreatingwell-
considered soil legacy effects. The paper explores both the direct use
of plants and the synergistic use of soil microorganisms to establish
positive soil legacy effects, offering innovative insights to boost
production potential and improve the ecological environment of
saline farmland. The emphasis lies on creating positive soil legacy
effects through the selection of suitable salt-tolerant crops, the
development of planting patterns with a rational match of crop
functional groups, the inoculation of functional microorganisms, the
inoculation of safe and efficacious soils, and the application of advanced
agricultural technologies and bio-cultivation methods. This approach
underscores the practical utility of crop-soil microorganism interactions
Ma et al. 10.3389/fpls.2024.1396754
Frontiers in Plant Science frontiersin.org08
in agricultural production. In addition to plants and associated soil
microorganisms, the role of soil animals in constructing soil food webs is
acknowledged. These soil animals, through direct or indirect
interactions with microorganisms and plants, contribute to the cycling
of soil nutrient resources, influencing soil ecosystem function (Du et al.,
2018). Multi-trophic interactions between mycorrhizal fungi, fungus-
eating protozoa, and nematodes in the soil can enhance crop nutrient
uptake,cropyield,andtolerance(Jiang et al., 2020). This suggests that
future studies can more precisely and directly leverage soil legacy effects
to trigger positive tolerant responses by regulating specificspeciesorsoil
fauna in the soil food web of saline farmlands, or even by controlling
certain trophic levels.
Author contributions
YM: Writing –original draft, Writing –review & editing. CZ:
Funding acquisition, Writing –review & editing. YB: Funding
acquisition, Writing –review & editing. CS: Funding acquisition,
Writing –review & editing. FZ: Funding acquisition, Supervision,
Writing –review & editing.
Funding
The author(s) declare financial support was received for the
research, authorship, and/or publication of this article. This work
was supported by the Young Scientists Project of National Key
Research and Development Program of China (2021YFD1900200),
the National Key Research and Development Program of China
(2022YFF1302800, 2022YFD1900300), the Strategic Priority
Research Program of Chinese Academy of Sciences
(XDA26040103), the Special Key Grant Project of Technology
Research and Development of Zhangjiakou City (“Take-and-lead”
Program) (No.2022J001) and the “100 Talents Project”of Chinese
Academy of Sciences.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the
authors and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed or
endorsed by the publisher.
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