Plant Growth Regulation (2024) 103:271–281

https://doi.org/10.1007/s10725-024-01124-2

REVIEW ARTICLE

Elucidating the mechanism regarding enhanced tolerance in plants to

abiotic stress by Serendipita indica
Yu-Xi Wan1 · Rupam Kapoor2 · Fábio Sérgio Barbosa da Silva3 · Elsayed Fathi Abd-Allah4 · Kamil Kuča5 ·
Abeer Hashem6 · Qiang-Sheng Wu1,5

Received: 30 October 2023 / Accepted: 11 December 2023 / Published online: 22 January 2024
© The Author(s), under exclusive licence to Springer Nature B.V. 2024

Abstract
Seredipita indica (formerly Piriformospora indica) is an endophytic fungus that establishes the symbiosis within the roots
of various plants, exhibiting analogous functions to arbuscular mycorrhizal fungi. S. indica can proliferate in vitro in
synthetic media, without the need of a host. Due to its isolation from desert environments, S. indica is particularly promi-
nent in enhancing the host plant’s tolerance to abiotic stresses. This review briefly analyzes the role of S. indica in plants
exposed to abiotic stresses (e.g., drought, waterlogging, salt stress, low temperatures, and heavy metal stress). This review
also elucidates the underlying mechanism regarding S. indica-enhanced tolerance of host plants in response to abiotic
stress by regulating nutrient acquisition, osmoregulation (proline, soluble sugars, betaine, and K+), phytohormone (aux-
ins, abscisic acid, ethylene, and gibberellins) balance, antioxidant enzyme defense systems, polyamines (e.g., putrescine),
and functional genes (e.g., aquaporins and phosphate transporter). Some of the fungus’ own genes, such as transporters
of polyamines, also respond to abiotic stresses, thereby assisting the host in co-resistance to abiotic stresses. The review
further examines the application potential of S. indica to enhance stress tolerance in the field as well as proposes future
prospects (e.g., omics, fungal self-response, reactive oxygen species signalling transduction, and its association with other
microorganisms).

Keywords Antioxidant defense system · Drought stress · Endophytic fungi · Environmental management · Functional
genes · Salt stress

Introduction
Communicated by Ben Zhang.

Qiang-Sheng Wu Abiotic stress refers to the negative effects of abiotic

wuqiangsh@163.com factors on plant growth and development. As a result of
global warming, various extreme environments such as
1
College of Horticulture and Gardening, Yangtze University, prolonged drought, high temperatures, and extreme pre-
Jingzhou, Hubei 434025, China
cipitation occur, exposing crop growth to abiotic stresses
2
Department of Botany, Faculty of Science, University of (Aguilar and Lozano-Duran 2022). Abiotic stress has led
Delhi, Delhi 110007, India
to a decline in crop yields and farmed areas, threaten-
3
Laboratory of Analysis, Research and Studies in ing the global food supply. Soil drought, for example,
Mycorrhizae—LAPEM, Research Center of the Institute
of Biological Sciences—ICB, University of Pernambuco— affects 45% of arable land worldwide, while soil salinity
UPE, Rua Arnóbio Marques, 310, Santo Amaro—Recife, can negatively affect crop yields by 10–50% (Godoy et
Pernambuco 50100-130, Brazil al. 2021). In addition, heavy metal contamination of soil
4
Plant Production Department, College of Food and caused by human activities further inhibits crop growth
Agricultural Sciences, King Saud University, Riyadh and yield. It is consequently critical to strengthen plants’
11451, Saudi Arabia adaptive capacity to cope with abiotic stresses.
5
Faculty of Science, Department of Chemistry, University of Some fungi can be symbiotic in plants, forming a mutu-
Hradec Kralove, Hradec Kralove 50003, Czech Republic ally beneficial association with the plants (Peter et al. 2011).
6
Botany and Microbiology Department, College of Science, When plants are subjected to abiotic stresses, symbiotic
King Saud University, Riyadh 11451, Saudi Arabia

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272 Plant Growth Regulation (2024) 103:271–281

fungi such as mycorrhizal fungi and endophytic fungi (e.g., as cell division, chlorophyll content, transpiration, and pho-
Seredipita indica) in roots respond to the stresses (Atkinson tosynthesis (He et al. 2020). However, root colonization of S.
and Urwin 2012; Khalid et al. 2019). S. indica was discov- indica has been demonstrated to mitigate drought damage in
ered in the roots of scrubby woody plants (Prosopis juliflora host plants (Table 1). Moreover, soil drought induced a sub-
and Zizyphus nummularia) in India’s Thar Desert (Verma et stantial increase in the colonization rate of S. indica in roots,
al. 1998). S. indica has been applied to Arabidopsis, maize, accompanied by an increase in the density of transparent
tobacco, barley, rice, poplar, white clover, citrus, etc., mostly pear-shaped spores, which further demonstrated the active
colonizing the root epidermis and cortex of the host plant adaptability of S. indica to drought (Wang et al. 2023b).
(Waller et al. 2005; Vadassery et al. 2008). In barley, S. indica Klute (2011) discovered that in the early stages of symbio-
predominantly colonizes root meristematic zones, with the sis of S. indica with host plants, intracellular Ca2+ levels
majority of the hyphae present in dead cells (Deshmukh et al. in host plants played an important role in early signalling
2006). After symbiosis with the host plant, S. indica exhibits processes. Cell wall extracts from S. indica promoted the
properties similar to those of arbuscular mycorrhizal fungi, increase in transient Ca2+ levels in cytoplasm of Arabidop-
such as helping host plant growth and development, improv- sis and tobacco plants (Vadassery et al. 2009a). It is known
ing fruit quality and nutrient uptake, and enhancing defense that Ca2+, as an important second messenger, is sensed by
against abiotic stresses (Yang et al. 2021; Boorboori and calmodulin and forms a complex that binds a variety of
Zhang 2022; Cheng et al. 2022; Saleem et al. 2022). Addi- transcription factors, resulting in an increase in cytosolic
tionally, endophytic fungi modify microbial defense path- membrane-associated Ca2+-sensing regulator (CAS) mRNA
ways and phytohormone levels to enhance defense against levels in S. indica-inoculated Chinese cabbages (Sun et al.
pathogens (Kundu and Vadassery 2022). 2010), which modulates downstream target genes involved
A typical role of S. indica in coexistence with plants is to in regulating the response to abiotic stresses. Furthermore,
increase host plant tolerance to abiotic stresses such as salt Vadassery et al. (2009b) found that S. indica enhanced anti-
stress, drought stress, and low temperature stress (Deshmukh oxidant capacity of host plants by activating the glutathione
et al. 2006; Zarea et al. 2012; Ansari et al. 2013a; Saleem et cycle, thereby increasing plant tolerance to drought stress.
al. 2022). S. indica can adapt to unfavourable environments As a result, the fungus plays an important role in enhanc-
such as soil nutrient deficit, high temperatures, pH levels, ing drought tolerance in plants. Yaghoubian et al. (2014)
and high concentrations of heavy metals (Yaghoubian et al. also investigated the effect of single and co-inoculation
2019). The fungus also modulates stress-responsive genes with AMF (Glomus mosseae) and S. indica on drought tol-
and nutrient acquisition to assist the host plant survive under erance of wheat plants. They observed that co-inoculation
unfavourable environments (He et al. 2020). The endo- with AMF and S. indica increased catalase (CAT), ascorbate
phytic fungus S. indica colonizes host plants for beneficial peroxidase (APX), and peroxidase (POD) activity, but the
effects, suggesting involvement in general recognition and increase was between two single inoculations.
signalling pathways. Unlike arbuscular mycorrhizal fungi,
this fungus not only colonizes non-mycorrhizal plants, but Salt stress
also it is capable of axenical culture without the need for
plant roots, leading to widespread interest in the fungus as a Salt stress causes leaf stomatal closure and decreases photo-
biostimulant in modulating stress responses of host plants. synthesis, which has a detrimental impact on nutrient uptake,
Many achievements have been accomplished in the study transportation, and distribution (Qi et al. 2020), resulting in
of S. indica colonization on regulating plant resistance to stunted growth and decreased yield. Inoculation of S. indica
abiotic stresses. This review attempts to elucidate the func- under salt stress considerably increased stomatal conduc-
tions of S. indica in enhancing abiotic stress resistance in tance and transpiration rate of maize (Yun et al. 2018).
plants, with an emphasis on which abiotic stresses S. indica Similarly, changes in the expression of several salt-tolerated
responds to and how S. indica enhances abiotic stress resis- genes revealed an important role of S. indica in enhanc-
tance in plants. ing plant salt tolerance. S. indica inoculation increased the
expression of salt tolerance-related genes SNAC1, OsNAC6,
S. indica-mediated effects on host plants under OsBZIP23, and OsDREB2A in the leaves of salt-stressed
abiotic stresses rice, resulting in improved salt tolerance (Liu et al. 2019). S.
indica improved tomato plant salt tolerance by boosting the
Drought stress uptake of nutrients such as N, P, and Ca, as well as modulat-
ing the expression of NHXs, SOS1, and CNGC15 in roots
Drought stress not only reduces crop growth and yield, but (Table 1) (Ghorbani et al. 2019), which thus improved salt
also disrupts physiological and biochemical processes such tolerance to S. indica-inoculated tomato.

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Table 1 Effects of Seredipita indica on stressed response in host plants

Stress Plants Nutrient Other physiological response Gene expression response References
types response
Drought Tobacco – Soluble protein↑; proline↑; malondialdehyde↓ NTNAC1↑; NAC4↑ Li et al. (2023b)
stress Sage – Root colonization rate↓; chlorophyll index↑ BPPS under 70% of field Aslani et al.
capacity↓; GPPS under70% of (2023)
field capacity↓; GPPS under
40% of field capacity↑
Maize – Catalase↑; superoxide dismutase↑; proline↑; CBL1↑; RD29A↑ Xu et al. (2017)
malondialdehyde↓
Salt Tomato N↑; P↑; Net photosynthetic rate↑ SOS1↑; CNGC15↑ Ghorbani et al.
stress Ca↑; K↑ (2019)
Alfalfa Na↓ Malondialdehyde↓; proline↑ P5CS2↑; PR1↑; PR10↑ Li et al. (2017)
Tobacco – Malondialdehyde↓; proline↑ OPBP1↑; PR-1a↑; PR3↑; Hui et al. (2014)
Water- Peach – Cadaverine↓; spermidine↓; putrescine↓; proline↑ SiTPO1↑; SiTPO2↑; SiTPO4↑ Liang et al.
logging (2023b)
stress Chinese – Superoxide dismutase↑; catalase↑; soluble sugar↑ – Yang et al.
cabbage (2014)
Rice – Malondialdehyde↓; catalase↑ – Tsai et al. (2020)
Low- Banana – Hydrogen peroxide↓; malondialdehyde↓; superoxide CSD1C↑; CBF7-1↑; ADA1↓; Li et al. (2021)
temper- dismutase↑; catalase↑ KIN10↓
ature Passion – Catalase↑; superoxide dismutase↑; hydrogen – Liang et al.
stress peroxide↓ (2022)
Arabidopsis – Soluble protein↑; proline↑; hydrogen peroxide↓ CBFs↑; CORs↑; SAG1↑; Jiang et al.
PYL6↑ (2020)
Heavy Tobacco N↑; P↑; Malondialdehyde↓; proline↑; catalase↑; peroxidase↑ PR-1a↑; PR2↑; PR5↑; PR1b↑ Guo (2019)
metal Zn↑
stress Alfalfa – Soil urease↑; soil sucrase↑ PR10↑; SRG↑ Zhu et al. (2019)
Sudangrass – Catalase↑; superoxide dismutase↑; glutathione↑; – Xian et al.
ascorbic acid↑ (2022)
Note: ↑ and ↓indicate significant increase and decrease in parameters after S. indica colonization, respectively.—means that this parameter is
not determined

Waterlogging stress al. 2020). S. indica inoculation in peach plants maintained

a better growth rate of the host under waterlogging through
Waterlogging has detrimental effects on soil physicochemi- mediating indoleacetic acid levels and also increased root
cal properties such as redox potential, pH value, and O2 proline levels, which was accompanied by an increase in
levels, allowing plant roots to experience hypoxic condi- Δ1-pyrroline-5-carboxylate synthetase 2 gene expression
tions, which in turn restricts plant growth, development, and an increase in leaf water potential (Liang et al. 2023a,
and survival (Parent et al. 2008). Interestingly, waterlog- b). These findings suggest that S. indica can be employed
ging treatment elevates the colonization of S. indica in as a biostimulant to improve host waterlogging tolerance,
host roots while simultaneously causing a massive accu- but the evidence and underlying molecular mechanisms lag
mulation of pear-shaped chlamydospores in roots (Liang behind those of drought and salt tolerance under S. indica.
et al. 2023b). Pear-shaped chlamydospores store O2 for
waterlogged roots. S. indica as a biostimulant has shown Low-temperature stress
beneficial effects in mitigating adverse effects of waterlog-
ging stress on plants (Li et al. 2023a). The application of Low temperatures can damage plant cell membranes and
S. indica in solid/liquid form could significantly increase produce secondary stresses such as osmotic stress and
the yield of waterlogged Chinese cabbage, as well as the oxidative stress, thus, restricting plant development and
protein, vitamin C, total soluble sugar, and chlorophyll con- potentially causing plant death (Sun 2022). In symbiosis
tents, thus reducing the waterlogged damage of Chinese with horticultural plants, S. indica can grow at low tempera-
cabbage, accompanied by a prominent effect of S. indica tures ranging from − 30 °C to 4 °C, indicating the ability
liquid fertilizer (Yang et al. 2014). In addition, inoculation of S. indica to improve plant tolerance to low temperature
with S. indica caused an increase in the activities of catalase (Table 1) (Wang 2015). The levels of soluble sugars, sol-
and glutathione reductase in rice under waterlogging stress, uble proteins, and proline were significantly increased in
thereby, improving their tolerance to waterlogging (Tsai et low-temperature stress after inoculation with S. indica in

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passion plants, implying that S. indica promotes the synthe- stress-tolerant genes in plants, which thus enhances the
sis of new proteins and sugars in the host to a certain extent plant defense response against heavy metal stress. However,
for reduced low-temperature damage (Liang et al. 2022). S. co-inoculation with AMF (Rhizophagus intraradices) and S.
indica colonization of Arabidopsis thaliana increased tol- indica did not show prominent effects in increasing proline
erance to low-temperature stress and accelerated recovery levels and decreasing malondialdehyde levels in soybeans
via up-regulating the expression of CBF and COR genes grown under high Cd conditions than single inoculation
(Jiang et al. 2020). Furthermore, S. indica up-regulated tran- (Wang et al. 2023a). Majooni Heris et al. (2022) reported
scription factors such as WRKY, ERF, and MYB in frozen that combined inoculation of AMF (R. intraradices) and S.
Arabidopsis seedlings (Jiang et al. 2021). Therefore, root indica resulted in higher chlorophyll levels in lettuce than
colonization of S. indica during low-temperature stress has single inoculation under Cd stress, accompanied by nutri-
a positive effect on host resistance. ent and anthocyanine levels that were not as prominent.
Hence, AMF and S. indica co-inoculation presents variation
Heavy metal stress in enhanced heavy metal stress, which is correlated with
the presence of the same competitive sites in roots and host
Heavy metals in soil not only pollute the environment, photosynthates.
but also have a detrimental impact on plant growth and In short, inoculation with S. indica can trigger physi-
development of plants, causing photosynthesis disruption, ological and molecular responses in the host plant exposed
physiological imbalance, and oxidative damage (Edelstein to abiotic stresses (Fig. 1), which thus enhances the host
and Ben-Hur 2018). The endophytic fungus S. indica pro- plant’s ability to resist abiotic stresses.
tects against heavy metal stress (Table 1) (Guo 2019). S.
indica boosted the levels of chlorophyll a, chlorophyll b, Underlying mechanisms regarding enhanced
and total chlorophyll in plants under Cd and Cu stress (Hui resistance in plants to abiotic stress by Serendipita
2014; Guo 2019). The expression of pathogenesis-related indica
protein genes and chitinase genes in tobacco was up-reg-
ulated by S. indica inoculation under Cd, Cr, and Pb stress Regulation of hormone homeostasis
(Wu 2014). Similarly, in rice under Cd stress, S. indica up-
regulated the expression of OsHMA3, a Cd-specific protein An important role for endogenous hormones is to regulate
gene that mediates compartmentalization in vacuoles, while growth, root development, and stress response in plants
it down-reguled the expression of OsHMA2, an export-type (Canales et al. 2023). S. indica triggered a large num-
transporter protein gene, which reduced the distribution of ber of differentially expressed genes in drought-stressed
Cd into the aboveground part of rice (Singhal et al. 2017). maize that annotated hormone functions, including aux-
As a result, S. indica induces the expression of heavy metal ins (Auxs), cytokinins, abscisic acid (ABA), and salicylic

Fig. 1 Plant typical response to

inoculation with Seredipita indica
under abiotic stress

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acid (Canales et al. 2023). Among them, indoleacetic acid response (Azizi et al. 2021). Such a mechanism needs to be
(IAA) as a compatibility factor is involved in the symbio- further explored.
sis (Tian et al. 2018). The improvement of host growth
by S. indica is associated with the up-regulated expression Improvement of osmotic adjustment
of IAA synthesis- and transport-assiciated genes, which in
turn triggers high levels of IAA for plant growth (Liu et Proline is an osmoprotectant that stabilizes cell membrane
al. 2023). Under salt stress, Kord et al. (2019) identified and protein structure, reduces photodamage to thylakoid
a miR167 (a target gene encoding auxin response factors) membranes, and regulates water potential (Ozturk et al.
whose abundance was reduced by S. indica colonization 2020). The impact of S. indica on host proline levels under
in rice, thereby promoting auxin response factor transcript abiotic stress has shown two trends: (i) under drought
levels for improved growth in stressed plants. A similar stress and osmotic stress, proline levels of S. indica-inoc-
phenomenon was also found in waterlogged peach seed- ulated plants are elevated (Saddique et al. 2018; Magh-
lings under S. indica colonization conditions (Liang et al. soudi et al. 2018; Azizi et al. 2021), which is associated
2023b). with Δ1-pyrroline-5-carboxylate synthase (P5CS) overex-
ABA is a stress hormone implicated in abiotic stress pression (Pooja et al. 2021; Liang et al. 2023b). S. indica
responses, including S. indica-modulated stress resistance also promoted the accumulation of proline in alfalfa leaves
in host plants (Xu et al. 2019). In maize, inoculation with S. under Cd stress and thus alleviated plasma membrane per-
indica increased the expression of the ZEP gene, a key gene oxidation (Liu et al. 2022). S. indica in combination with Zn
for leaf ABA synthesis to improve drought tolerance (Xu treatment could further increase the level of grape proline
et al. 2018). Under cold stress conditions, inoculation with in low-temperature stress to minimize the stress damage
S. indica significantly increased leaf ABA levels in grape- on cell structure and function, which improves cell mem-
vines (Karimi et al. 2022). S. indica could up-regulate the brane stability and osmoregulation (Karimi et al. 2022). (ii)
expression of the miR159 under drought stress, which in S. indica-inoculated plants show a decrease in proline lev-
turn down-regulated MYB transcription factor for reduced els under abiotic stress, which is related to a decrease in
programmed cell death, associated with the ABA signalling ABA levels (Camilo and Gomes 2010), or inoculated plants’
(Mohsenifard et al. 2017). resistance is increased without the need for the plant to syn-
Ethylene, a phytohormone, regulates plant growth and thesize more proline in response.
development as well as tolerance to abiotic stresses (Singh In osmotic adjustment, soluble sugars also prevent cell
et al. 2022). S. indica fails to colonize overexpressed-ERF1 osmotic imbalance and maintain cell membrane integ-
(ethylene response transcription factor) transgenic plants rity during stress (Heuer 2003). Elevated levels of soluble
(Wang 2015). If the ethylene signalling pathway is dis- sugars were found in salt-stressed rice (Liu et al. 2019),
rupted, the colonization of S. indica is reduced accordingly, as well as drought-stressed stevia (Nabizadeh et al. 2023)
demonstrating that ethylene is required for the colonization following inoculation with S. indica. Interestingly, in salt-
process of S. indica (Khatabi et al. 2012). Under salt stress, stressed tomato, S. indica inoculation had no significant
inoculation with S. indica altered metabolic and transcrip- effect on root soluble sugar levels, but reduced leaf soluble
tional processes in barley leaves, including the ethylene bio- sugar levels (Ghorbani et al. 2018). This is due to the fact
synthesis pathway (Ghaffari et al. 2016). Zarea et al. (2013) that S. indica symbiosis requires sugars, thereby, causing
therefore claimed that S. indica is able to modulate ethyl- a decrease in photosynthetic products in inoculated plants’
ene biosynthesis, particularly through the enhancement of leaves. In addition, S. indica inoculation increases betaine
1-aminocyclopropane-1-carboxylate activity. Increased eth- levels and K+/Na+ ratio under abiotic stresses, especially
ylene levels under S. indica induce the expression of various salt stress, thereby stabilizing the osmotic balance in the
stress-related genes via the ethylene signalling transduction host and enhancing its ability to retain water (Ghorbani et
pathway, thereby enhancing plant stress response (Gao et al. 2018).
al. 2020).
In addition, S. indica generates GA3 to improve host Polyamine regulation
growth and response to heavy metal-contaminated soils
(Ansari et al. 2013b). Drought stress increased the expres- Polyamines are aliphatic compounds comprising two
sion level of the GAI gene in tomato, a negative feedback or more amino groups (Gonzalez et al. 2021) and play
regulator of the GA signalling pathway, which reduces plant a crucial role in various stress responses within plants
growth; however, the inoculation of S. indica had no effect (Podlešáková et al. 2018). Metabolomic analysis of tomato
on the expression of the GAI gene, indicating that S. indica inoculated with S. indica revealed that putrescine was
does not modulate the GA signalling pathway in the stress most significantly induced in roots during the interaction

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between the host and S. indica, which was attributed to Regulation of stressed genes
S. indica-induced expression of arginine decarboxylase
1 (SlADC1) for putrescine biosynthesis pathway (Kundu Aquaporins (AQPs) are a class of intrinsic proteins pres-
et al. 2021). Thus, putrescine is necessary for S. indica to ent in the plasma membranes or vesicle membranes, and the
mediate plant growth promotion. S. indica significantly regulation of their activity is a mechanism of plant adap-
increased putrescine, spermidine, and spermine levels in tation to abiotic stress (Kapilan et al. 2018). S. indica had
grapevine leaves when subjected to cold stress (4 °C), two responses to AQP expression in host plants under abi-
and the positive effect can be amplified by the addition otic stress: (i) S. indica down-regulates the expression of
of zinc chelate. S. indica, on the other hand, significantly AQPs in host plants, leading to decreased membrane perme-
suppressed putrescine, cadaverine, and spermidine levels ability and increased cellular water retention (Maurel et al.
in waterlogged peach roots, and the polyamine altera- 2015). For example, the expression of the PIP2;5 gene was
tion was correlated with the up-regulation of polyamine decreased in oilseed rape under salt stress after inoculation
uptake transporter 2 (PpPUT2), PpPUT5, and PpPUT6 with S. indica (Sairebieli 2022). (ii) S. indica up-regulates
expression by S. indica (Liang et al. 2023b). Hence, S. the expression of AQPs in host plants under abiotic stress,
indica-mediated polyamines in response to abiotic stress thereby enhancing water uptake (Ghorbani et al. 2018). For
vary and may depend on the host plant as well as the type example, root colonization of S. indica under salt stress
of stress. Further work is needed to clarify how S. indica increased the expression of NIP6;1 in Gerbera jameso-
mediates the role of polyamines and γ-aminobutyric nii, preserving plant cellular water homeostasis (Chen et
acid (a downstream product of polyamines) in the stress al. 2022). However, inoculating S. indica under salt stress
response. up-regulated the expression of PIP1;2 and PIP2;4 genes in
tomato, while exhibiting no significant impact on the expres-
Enhancement of antioxidant defense systems sion of TIP1;1 and TIP2;2 genes (Ghorbani et al. 2019).
This demonstrates the complexities of the AQPs family’s
Abiotic stresses can cause an oversupply of reactive oxy- transcriptional regulation under S. indica colonization.
gen species in plants, resulting in oxidative damage to S. indica also overcomes shortages of Ca2+, Mg2+, K+,
2+
proteins, lipids, and nucleic acids (Hussain et al. 2019). Zn , Cu, and Fe in drought-stressed wheat plants and mini-
At the same time, enzymatic and non-enzymatic antioxi- mizes damage to cellular ultrastructure (Singh et al. 2023).
dant defenses are activated in plants in response to abiotic In maize, S. indica inoculation promoted 32P uptake, sug-
stresses (Akbar et al. 2023). Previous studies have dem- gesting that fungal mycelium transfers P to the host plant
onstrated that the endophytic fungus S. indica increases under P-deficient conditions (Kumar et al. 2011). The S.
the activity of antioxidant enzymes in host plants, conse- indica-mediated increase in host P acquisition originates
quently enhancing their tolerance (Table 1) (Guo 2019). from the fact that S. indica facilitates the release of acid
After inoculation with S. indica, the activity of superox- phosphatase from the host roots into the soil, solubilizing
ide dismutase (SOD), POD, CAT, glutathione reductase, insoluble P into soluble P for plant acquisition (Malla et al.
and APX was significantly elevated in drought-stressed 2004), along with up-regulation of Pi transport protein (PT)
trifoliate orange plants, thereby mitigating the oxidative genes (Rong et al. 2023). A gene (PiPT) encoding a high-
damage caused by drought to the host (Cao et al. 2022). affinity phosphate transporter protein has been identified in
Thus, inoculation with S. indica successfully activates S. indica (Yadav et al. 2021). Under P-deficient conditions,
the plant’s reactive oxygen species scavenging system, the expression of PiPT is activated, which is responsible
especially the ascorbate-glutathione cycle to reduce reac- for P transfer from the fungus to the host plant (Aslam et
tive oxygen species levels and alleviate plasma mem- al. 2019). Therefore, PiPT is an important component of P
brane peroxidation (Waller et al. 2005; Rong et al. 2022). transport at the S. indica-root interface, responding to nutri-
Furthermore, S. indica has been shown to increase the ent stress and enhancing plant growth (Yadav et al. 2021).
expression of CAT, APX2, and SOD genes in rice sub- However, the expression of PiPT is P-dependent, with PiPT
jected to salt stress (Xia et al. 2023). The expression inactive under P-rich conditions and overexpressed under
of Fe-SOD, Cu/Zn-SOD, POD, and CAT1 in trifoliate P-deficient conditions to transport high amounts of P to host
orange was up-regulated by inoculation with S. indica plants (Kumar et al. 2011). It will be interesting to deter-
under drought stress (Wang et al. 2023b). As a result, root mine whether PT genes from both the host and S. indica
colonization by S. indica activates the host antioxidant synergistically or competitively promote host P acquisition
defense system at both physiological and molecular lev- under abiotic stresses, especially nutrient stress.
els, thereby increasing plant tolerance to abiotic stresses In addition to AQPs and PTs, other functional and regu-
(Fig. 1). latory genes are implicated in S. indica events (Table 1).

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Plant Growth Regulation (2024) 103:271–281 277

For example, the expression of SOS1 and CNGC15 was up- in central Europe, but it is more suitable for tropical or sub-
regulated by S. indica in tomato under salt stress (Ghorbani tropical agriculture (Serfling et al. 2007).
et al. 2019); Fe-SOD, Cu/Zn-SOD, FAD2, and FAD6 genes In addition to the positive effects observed with the myce-
were up-regulated by S. indica in drought-treated trifoliate lium and spores of S. indica, cell wall extracts and culture
orange as well as CAT and APX2 in salt-stressed maize (Cao filtrates of S. indica have shown positive benefits for plant
et al. 2022; Xia et al. 2023). Liang et al. (2023b) further growth (Upadhyaya et al. 2013). Moreover, S. indica has
identified four transporters of polyamine (TPO) in S. indica been mixed with a carrier, magnesium sulphite, to develop a
and found that the expression of SiTPO1, SiTPO2, and biofertilizer, rootonic, which has been used in the field as a
SiTPO4 was up-regulated by waterlogging. Nevertheless, source of bioinoculants (Saleem et al. 2022). This provides
how SiTPOs and plant PUTs are involved in the waterlog- a guarantee for the large-scale application of S. indica in
ging response in roots is unknown. the field.

S. indica as a field enhancer of plant stress tolerance

Conclusions and perspectives
The rapid and large-scale propagation of S. indica in vitro
allows its inoculants to be used in the field, making it attrac- The endophytic fungus S. indica colonizes non-mycor-
tive for agroforestry, horticulture, and medicinal plants rhizal plants and has a diverse host range. Its effects are
(Oelmüller et al. 2009). Sustainable agriculture requires a analogous to those of arbuscular mycorrhizal fungi, mak-
reduction in the input of inorganic fertilizers and pesticides, ing it an excellent candidate as a friendly biostimulant to
making plant growth-promoting fungi including S. indica of enhance plant tolerance to abiotic stresses. The majority of
special interest (Karuna et al. 2023). In addition, S. indica the experiments confirmed S. indica’s positive effects on
has been utilized to identify target genes and fungal effec- abiotic stress tolerance in host plants, and this effect was
tors for plant stress response, thus providing materials for associated with the optimization of endogenous hormone
subsequent resistance breeding (Oelmüller et al. 2009). Li homeostasis, improved nutrient uptake, enhancement of
et al. (2022) found that inoculating S. indica into the rhi- antioxidant enzyme defense system, modulation of poly-
zosphere of field lane late navel orange trees significantly amine metabolism, and activation of the expression of some
increased SOD, POD, and CAT activity in leaves, ascorbic functional genes by S. indica. Although the intrinsic physi-
acid and glutathione levels, and POD, CAT1, and FAD6 ological mechanism regarding S. indica-enhanced stress tol-
expression. Thus, S. indica-inoculated plants initiate a sys- erance has been clarified, the hidden molecular mechanism
temic ‘defense readiness’ through the ascorbate-glutathione lags behind. Future research should focus on the following
cycle, better resistance to abiotic stresses, which results in aspects:
increased crop yields, such as a 10% increase in field barley
(Waller et al. 2005). S. indica was also applied to barley (i) Using omics such as transcriptomics, metabolomics,
in the field and a significant decrease in the disease index and proteomics to excavate differentially expressed
of Pseudocercosporella herpotrichoides was found in the genes and metabolites, so as to comprehensively reveal
inoculated plants, accompanied by an increase in the num- the intrinsic mechanism of enhanced host tolerance to
ber of sheath layers (Serfling et al. 2007). It suggests that abiotic stress modulated by S. indica;
the colonization of S. indica in roots initiates systemic resis- (ii) It is critical to clarify how S. indica itself responds
tance in plants. Khalvandi et al. (2019) applied S. indica on to abiotic stress, as earlier studies focused on plant
peppermint (Mentha piperita) and observed that S. indica responses to S. indica under abiotic stress.
mitigated the negative effects of salt stress on membrane (iii) How S. indica modulates the signalling pathway of reac-
electrolyte leakage and improved essential oil components tive oxygen species as well as the interaction between
such as menthone, and enhanced antioxidant capacity. In reactive oxygen species and phytohormones, goes to
addition, S. indica promotes the survival of micropropa- coordinate the plant’s response to abiotic stresses.
gated plantlets such as strawberry, tobacco, banana, and (iv) Other beneficial microbes that synergize with S. indica
sugarcane, which is associated with enhanced abiotic stress against abiotic stresses are needed for subsequent sus-
resistance (Tarte et al. 2022). Therefore, S. indica has a high tainable agriculture and environmental management.
potential for commercial plant tissue culture. However, in
crops with a long harvest period, such as tomatoes, S. indica Acknowledgements The authors would like to extend their sincere
only enhances yields for a limited time (Franken 2012), appreciation to the Researchers Supporting Project Number.
(RSP2024R134), King Saud University, Riyadh, Saudi Arabia.
suggesting that S. indica has a constraint. Nevertheless, S. The work was also supported from Excelence project PrF UHK
indica may not be well adapted to temperature conditions 2216/2023–2024.

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278 Plant Growth Regulation (2024) 103:271–281

Author contributions YXW and QSW: conceptualization and visual- Cheng XF, Xie MM, Li Y, Liu BY, Liu CY, Wu QS, Kuča K (2022)
ization; YXW: data curation and formalization; WYX: writing; RK, Effects of field inoculation with arbuscular mycorrhizal fungi
FSBS, EFA, KK, AH, and QSW: writing, review, and editing. All the and endophytic fungi on fruit quality and soil properties of
authors have read and agreed to the published version of this manu- Newhall navel orange. Appl Soil Ecol 170:104308. https://doi.
script. org/10.1016/j.apsoil.2021.104308
Chen WT, Lin FZ, Lin KH, Chen CM, Xia CS, Liao QL, Chen SP,
Kuo YW (2022) Growth promotion and salt-tolerance improve-
Declarations ment of Gerbera jamesonii by root colonization of Piriformos-
pora Indica. Plant Growth Regul 41:1219–1228. https://doi.
Conflict of interest The authors declare no conflict of interest. org/10.1007/s00344-021-10385-4
Deshmukh S, Hueckelhoven R, Schaefer P, Imani J, Sharma M, Weiss
M, Waller F, Kogel KH (2006) The root endophytic fungus Piri-
formospora indica requires host cell death for proliferation dur-
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