Archives of Microbiology (2020) 202:1581–1596

https://doi.org/10.1007/s00203-020-01915-x

MINI-REVIEW

The potential of arbuscular mycorrhizal fungi in C cycling: a review

Manoj Parihar1   · Amitava Rakshit2 · Vijay Singh Meena1 · Vijai Kumar Gupta3 · Kiran Rana4 · Mahipal Choudhary1 ·
Gopal Tiwari5 · Pankaj Kumar Mishra1 · Arunava Pattanayak1 · Jaideep Kumar Bisht1 · Surendra Singh Jatav2 ·
Priyanka Khati1 · Hanuman Singh Jatav2

Received: 23 October 2019 / Revised: 15 April 2020 / Accepted: 15 May 2020 / Published online: 24 May 2020
© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract
Arbuscular mycorrhizal fungi (AMF) contribute predominantly to soil organic matter by creating a sink demand for plant C
and distributing to below-ground hyphal biomass. The extra-radical hyphae along with glomalin-related soil protein signifi-
cantly influence the soil carbon dynamics through their larger extent and turnover period need to discuss. The role of AMF
is largely overlooked in terrestrial C cycling and climate change models despite their greater involvement in net primary
productivity augmentation and further accumulation of this additional photosynthetic fixed C in the soil. However, this buff-
ering mechanism against elevated C ­ O2 condition to sequester extra C by AMF can be described only after considering their
potential interaction with other microbes and associated mineral nutrients such as nitrogen cycling. In this article, we try to
review the potential of AMF in C sequestration paving the way towards a better understanding of possible AMF mechanism
by which C balance between biosphere and atmosphere can be moved forward in more positive direction.

Keywords  Nutrient exchange · Net primary productivity · Glomalin · Soil nitrifiers · Carbon sequestration

Introduction et al. 2014). SOC as the most ambiguous pool of global C

The soil organic carbon (SOC) as the largest component of
the terrestrial C pool has a significant impact on the earth’s
atmosphere and climate (Batjes 1996; Stockmann et  al.
2013). According to a study, soil carbon stock is estimated
to be 1500Pg of carbon which is higher than the atmospheric
and phytomass carbon combined together (Scharlemann
Communicated by Erko Stackebrandt.
* Manoj Parihar
manoj.parihar1@icar.gov.in; manojbhu7@gmail.com
1
ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan
(VPKAS), Almora, UK 263601, India
2
Department of Soil Science and Agricultural Chemistry,
Institute of Agricultural Sciences, Banaras Hindu University
(BHU), Varanasi, Uttar Pradesh 221005, India
3
School of Natural Sciences, National University of Ireland
Galway, Galway, Ireland
4
Department of Agronomy, Institute of Agricultural
Sciences, Banaras Hindu University (BHU), Varanasi,
Uttar Pradesh 221005, India
5
ICAR-National Bureau of Soil Survey and Land Use
Planning, Nagpur, Maharashtra 440033, India
cycle in terms of the amount stored in soil or emitted back
to the atmosphere is influenced significantly by the land use
and changes therein (van der Werf et al. 2009; Harris et al.
2012; Le Quéré et al. 2018). Therefore, it is of paramount
importance to understand the process of managing the accu-
mulation of carbon in soil with greater residence time to
predict the future climate change scenario. The SOC pool
primarily depends on phytomass productivity and distribu-
tion of photosynthetic fixed carbon to below or above ground
biomass (Zhu and Miller 2003), which in result regulates
the microbial community structure and related processes in
the soil (Mohammadi et al. 2011). Subsequently, the micro-
bial community also has an imperative function in efflux or
influx of soil C through respiration, decomposition, and min-
eralization and immobilization process. However, net soil C
dynamics will be decided by the interactive effect of climate,
edaphic factor, land use management and quality and extent
of C inputs in the soil system (Solaiman 2014). Recently,
some studies highlighted the role of plant-associated fungi in
C dynamics and suggested that they can sequester 70% more
carbon to the soil (Averill et al. 2014). However, to date, the
contribution of these plant fungus symbiotic association is
not much credited and has been given little importance in

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global climate models (Averill et al. 2014). Among these
plant associated and mutually benefited fungi, AMF is very
common and ubiquitous with most of the terrestrial plants
under different habitats (Wang and Qiu 2006; Smith and
Read 2008). The basis of this symbiosis between AMF and
plants roots is to satisfy the nutritional demands of each
other (Smith and Read 2008). In exchange of different low
diffusive nutrients such as ammonium ­(NH4,) phosphorus
(P), Zinc (Zn) and copper (Cu), AMF create a sink demand
for carbon (C) and facilitate 4–20% C drain from the plants
(Wright et al. 1998; Willis et al. 2013). This additional C
along with extensive mycelium of AMF have effects on
active soil C pool. According to Treseder and Cross (2006),
AMF structure inside the plant roots, excluding extraradical
hyphae (ERH) of AM fungi, contains approx. 0.5 Pg C in
the upper soil surface. Further, ERH dry weight also repre-
sents a significant portion of soil microbial biomass (SMB),
i.e. ~ 0.03 to 0.5 mg g−1 (Miller et al. 1995) constituting ~ 54
to 900 kg ha−1 SOC. This significant pool of C received by
AMF when incorporated into the soil could be a fulcrum for
mitigating climate change globally (Solaiman 2014) under
suitable management condition. In spite of the substantial
amount of carbon retained by AMF, mean residence time
of C in soil and its physical protection are crucial for its
prolonged storage in soil. In addition to this, under elevated
­CO2 condition, upregulation of photosynthesis via greater
sink demand and allocation of extra C to the soil system
will have some impact on soil inherent microbial commu-
nity which in turn regulates and contribute significantly in
terrestrial C flux.
In this review, first we discuss about carbon transfer
from plant to fungi and then present an overview on AMF
role in global C cycling with different mechanism that will
determine net C flux between biosphere and atmosphere.
Future climatic conditions also have some serious implica-
tions on the interaction of AMF and other associated soil
microbes to determine net soil C sequestration or turnover
which needs to be understood in detail. We conclude with
possible suggestions for future research to facilitate greater
AMF-mediated C sequestration in soil system.
AMF mediated C flux between plant and soil
From various research studies, now it has been clear that
AMF colonization in plant roots create a sink demand for
carbon and significant proportion of this plant fixed C is
allocated to fungi. However, before reviewing the C seques-
tration potential of AM fungi, the translocation of C from
plant to AM fungi needs to be understood well. The AMF
root colonization with host plant to form symbiosis for the
transfer of nutrient and C between two is achieved through
the chemical transmission. In response to plant signal
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Archives of Microbiology (2020) 202:1581–1596
(strigolactones) received by AM fungi, germination of spore
is induced and its growing hyphae move towards the host
roots and form physical contact with host plant roots with
the help of hyphopodia. By initiating a series of reprogram-
ming, AM fungal hyphae penetrate the host epidermal cell
by forming pre-penetration apparatus (PPA) as a guide and
subsequently grow inside the root cortical cell. Inside the
cortical cell, it forms a highly branched tree-like structure
called arbuscular surrounded by a periarbuscule membrane
(PAM) which separates it out from the cytoplasm of the
host plant. These branched arbuscules are primarily respon-
sible for nutrient exchange between plant and AM fungi and
facilitate the carbon influx (Parniske 2008; Wang et al. 2017;
Wipf et al. 2019). Recently, it has been shown that in addi-
tion to sugar, host plant-synthesized lipids are also trans-
ferred directly to AMF. However, the relative contribution of
carbon transfer as a lipid or sugar still needs to be quantified.
Sugar channelization from host plant to AM fungi
As it is well known that AMF increase the availability as
well as accessibility of nutrient and water for host plants
in lieu of which host plants channelize about 4–25% of
their photosynthates towards AMF roots (Hobbie 2006).
Being the obligate biotrophs, AMF, without coloniza-
tion of host plants, are incapable of completing their
life cycle and sugar transport as well as its metabolism
forms an important pillar for understanding this behavior.
The flux of the carbon photosynthesised in plant leaves
towards AM colonized root is tightly controlled by both
partners. Earlier, starch was supposed to be important
for AMF symbiosis (Kinden and Brown 1975; Smith
and Gianinazzi-Pearson 1988) as AMF acquire all of its
required carbon from host during symbiotic period but
later, normal root colonization was also observed sig-
nificant in mutants impaired for starch degradation or
synthesis (Gutjahr et al. 2009, 2011). Since, AMF, as a
whole, are capable to uptake hexose from their host but
not sucrose (Bago et al. 2000), sucrose derived from host
needs to be splitted into usable hexose form for fungal
symbiont. However, due to differential structure and func-
tions, components of AMF vary in their role of hexose
metabolism. The sucrose-cleaving ability, a pre-requisite
to metabolize hexoses by AMF, is evidently absent in
extraradical mycelium of AMF (Pfeffer et al. 1999) which
negate the role of hexose sugar as energy source in this
part (Wipf et al. 2019), while in contrast, mechanism for
hexose metabolism is shown to exist in intraradical myce-
lium but this postulates of it being the ‘energy engine’
still needs confirmation (Pfeffer et al. 1999; Solaiman
and Saito 1997; Wipf et al. 2019). Contrary to symbiotic
phase, during pre-symbiotic period, AMF spore germina-
tion and initial hyphal growth are found to be independent
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of roots of host plant as established from the presence of

two mono-saccharide transporter (MST) in germinating
spores involved in direct uptake of sugar from the soil
(Ait Lahmidi et al. 2016).
Post-AM establishment period, sugar efflux from
plant to fungus is carried out either actively or passively
(Ho and Trappe 1973; Doidy et al. 2012a, b). Accord-
ing to Manck-Götzenberger and Requena (2016), sucrose
is transported via phloem to apoplast (cleaved there by
invertases and synthase) and is then unloaded into the
cortical cell of the root system for their further supply to
AM fungi. The different plant SUcrose Transporter (SUT)
proteins, as described in Table 1, present in mycorrhizal
roots play significant role in regulating the increase in C
partitioning and mycorrhizal root sink (Boldt et al. 2011;
Doidy et al. 2012b; Gaude et al. 2012). Apart from SUTs, Fig. 1  A model showing the transfer of sugar and lipids (16:0 C fatty
acid) from host plant to AMF arbuscule by using various transporters
sugar segmentation in AM is also facilitated by varied
range of plant and fungal sugar transporters (Casieri et al.
2013; Garcia et al. 2016). One such is MSTs that aid in Lipid transportation from host plant to AM fungi
transport of monosaccharides (glucose and fructose)
cleaved from sucrose by invertases and sucrose synthase Other than sugars, fatty acids (FAs), imported from host
present in host sink organs, primarily at the plant–fungus plants, are also the source of carbon for the AMF. Plants,
interface (Lalonde et al. 2004) to fungal partner. GpMST1 being accomplished with type I multi domain fatty acid syn-
and RiMST2 (Glomus sp.) were MSTs exhibiting glucose thetase (FAS 1) complex, can biosynthesize FAs de novo in
import activity in Glomeromycotan fungi (Schüßler et al. their plastids. On the other hand, AMF cannot synthesize
2006; Helber et al. 2011). Other is recently identified FAs without the existence of the host as they lack FAS 1
plant transporter Sugars Will Eventually be Exported complex rendering them reliant on plant host for de novo
Transporters (SWEETs) which is characterized as both synthesis of FAs, which could be a probable explanation for
exporter and importer of sucrose and monosaccharide obligate biotrophic behavior of AMF (Wipf et al. 2019). In
from/to protoplast (Chen 2014). addition, de novo FAs synthesis has been observed only in
Furthermore, different studies suggest that coloniza- the AMF symbiosis forming plants which further substanti-
tion by AMF enhances the activity of alkaline invertase, ate the FA auxotrophy of AMF (Bravo et al. 2016; Jiang
thus, making hexose available for AMF development et al. 2017) and transport of lipid from plants to AMF for
(Schubert et al. 2004). Following the acquisition of the maintaining colonization. Interestingly, genomes present in
carbon by AM fungi from host plant, it is transported AMF do encode the enzymatic system necessary for elon-
to extraradical mycelium (ERM) through intra radical gation of 16:0 FAs and their desaturation (Trepanier et al.
mycelium (IRM) for the production of spore and hyphal 2005; Wewer et al. 2014) suggesting that said functions in
growth (Fig. 1). AMF are independent of host. Lipids, while participating in

Table 1  List of various transporters involved in carbon transfer from the host plant cell to AMF arbuscule
Transporter Location Plant/mycorrhizal sp. Nutrient References

SUT Plant cell (leaf and root cell) Tomato Sugar Boldt et al.(2011)
SUTs, MST Plant cell Medicagotruncatula Sugar Doidy et al. (2012b) and Gaude et al. (2012)
SWEETs Plant cell (roots) Potato Sugar Manck-Götzenberger and Requena (2016)
STR, STR2 PAM Medicagotruncatula Lipids Zhang et al. (2010) and Jiang et al. (2017)
STR1, 2 PAM Rice Lipids Gutjahr et al. (2012)
GpMST1 Fungal symbiotic membrane Geosiphonpyriformis Monosaccharide Schüßler et al. (2006, 2007)
RiMST2 Intraradical fungal structure Glomus sp. Sugar Helber et al. (2011)

SUT sucrose transporter, MST MonoSaccharide transporter, SWEETs sugars will eventually be exported bu transporter, STR stunted arbuscule,
GpMST glomeromycotan monosaccharide transporter, RiMST monosaccharide transporters from rhizophagus irregularis, PAM periarbuscular
membrane

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C efflux from plants towards AMF symbionts (Luginbuehl
et al. 2017), form significant constituent of varied structures
such as spores (95% dry weight), extraradical mycelium
(47% hyphal volume), intraradical vesicles (58% dry weight)
and pre-symbiotic germ tubes (Bago et al. 2002). Lipids
are the major chunk of stored C-compounds in AMF which
store the carbon predominately in the form of triacylglycerol
(TAG) with 16:0 (palmitic acid) fungal fatty acids (FAs) as
a major component. With the development of arbuscule in
the plant cell, plastids increase in number with changes in
the position of endoplasmic reticulum to satisfy the growing
demands for lipids (Lohse et al. 2005; Ivanov and Harrison
2014). Two lipids biosynthesis genes acyl-ACP thio-ester-
ases (FatM) and reduced arbuscular mycorrhiza2 (RAM2)
and their importance for arbuscule development have been
demonstrated successfully in Medicago truncatula mutants
(Wang et al. 2012; Bravo et al. 2017). The FatM helps in the
termination of fatty acid chain elongation process by sepa-
rating the acyl carrier protein (ACP) from acyl group and
releasing soluble ACP and FAs (Jones et al. 1995). RAM2
encodes the glycerol-3-phosphate acyltransferase (GPAT)
which is important for AMF root colonization (Wang et al.
2012). In addition, half ATP-binding cassette transport-
ers  (ABC transporters) localized on the peri-arbuscular
membrane STR and STR2 (Zhang et al. 2010) are speculated
to transfer C16:0 2-monoacylglycerol (MAG) synthesized
by RAM2 towards arbuscules of AM fungi (Fig. 1) (Gut-
jahr et al. 2012; Bravo et al. 2017). RAM2 and STR are
transcriptionally regulated by a transcription factor reduced
arbuscular mycorrhiza1 (RAM1) (Park et al. 2015; Pimpri-
kar et al. 2016). However, mutations in FatM, RAM2 and
RAM1 impair arbuscule branching (Pimprikar et al. 2016)
and generally remain absent from plant genome that has
restricted the AMF colonization (Delaux et al. 2014; Bravo
et al. 2016). Transfer of host carbon to AM fungi in lipids
form could be an important mechanism where lipids contain
higher energy amount than per unit weight of carbohydrate.
Pathways of AMF‑mediated carbon
sequestration
The AMF receive their entire C demand from the host plant
and large part of this C is deposited in the soil as fungal
chitin or glomalin-related soil protein (GRSP). The fungal
and other microbial-derived C persist in soil for a longer
duration than plant originated C (Prescott 2010). GRSP
accounts for 30–40% of organic carbon in undisturbed soils
(Rillig et al. 2003) and it represents a large flux of SOC,
i.e. 10–100 g m−2 year−1 (Treseder and Turner 2007). AMF
mycelium also forms a large proportion of SMB and cal-
culated as 0.03–0.35 mg g−1 under linseed field (Olsson
et al. 1999) and 0.5 mg g−1 for a prairie community with
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111 m cm−3 hyphal length (Miller et al. 1995). According
to an estimate, 1 g of grassland soil contains ~ 100 m of
AMF hyphae (Johnson and Gehring 2007). Extramatrical
hyphae of AMF outside the plant root may constitute around
20–30% of SMB and 15% of SOC pool (Leake et al. 2004).
In another mechanism AMF contribution is likely to be mul-
tiplied by means of physical protection of SOM from decom-
position through better soil aggregation (Rillig 2004) and via
a general improvement in Net primary productivity (NPP) as
a major determinant for SOC (Hoeksema et al. 2010). Allo-
cation of C fixed through enhanced NPP in above and below
ground is a major factor for C sequestration and a significant
portion of belowground NPP, i.e. ~ 47% can be received by
AMF (Treseder 2016). Globally, AMF regulate the flow of
approximate 5 billion tons of carbon annually which form a
substantial part of C cycling (Bago et al. 2000). AMF con-
tribute significantly to enhance C storage in soil via adding
a copious amount of organic residue in the form of hyphal
biomass, GRSP and other hyphal exudates which release
organic C as and when decomposed and senesced. The major
sources of soil C which are regulated by AM fungi, as given
in Table 2, will be discussed in greater detail below.
Hyphal biomass
The AMF hyphae composition, extent and turnover rate
influence directly the soil carbon dynamics. Generally,
AMF contributes largely in soil C cycling due to their large
hyphal biomass, i.e. 20–30% of SMB (Leake et al. 2004) and
deposition of this C away from rhizosphere region of high
respiration activity. However, Staddon et al. (2003) found
that the average turnover time of ERH is 5–6 days only and
leads to its respiration back into the environment instantly.
Therefore, it is important to review the potential of ERH in C
sequestration in soil where it has very short turnover period.
Actually, the ERH cell wall is composed primarily of chitin,
i.e. a carbohydrate relatively recalcitrant in nature and in
some studies, it has been found that protein/amino acid/chi-
tin-derived pyrolysis products may persist for 49 ± 19 years
(Gleixner et al. 2002). Further, residual hyphal biomass also
contributed ~ 54–900 kg ha−1 soil organic carbon in stable
and recalcitrant pool which is functionally important for C
sequestration. In addition to this, interaction of the soil parti-
cles with AMF hyphal biomass form water stable aggregates
and provides physical protection to soil C from microbial
degradation (Zhu and Miller 2003). Inspite of the rapid
turnover of ERH, they form a significant proportion of the
soil carbon (Miller et al. 1995) indicating the existence of
various ERH pool based on their architecture (Staddon et al.
2003). Possibility of the existence of various ERH pools
which differ in turnover period suggests for reconsideration
of their contribution in C sequestration separately.
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Table 2  Extent of various AMF-derived carbon sources reported under different studies

Land use/Exp. type AMF carbon source Amount Plant/mycorrhizal sp. References

Tropical rainforest GRSP Chiapas 1.04–12.24 and at Mostly Acaulospora and Violi et al. (2008)
Veracruz 2.85–6.45 mg g−1 Glomus
soil
Tropical rain forest GRSP 3.94 ± 0.16 mg cm−1 3.2% of Acaulosporamorrowaie A. Lovelock et al. (2004)
total soil C and 5% of soil Mellea and A. foveata
nitrogen
Tropical soils GRSP 60 mg cm−3 Gigasporarosea or Glomus- Rillig et al. (2001)
intraradices
Forest soil EM mycelium 700–900 kg ha−1 Ectomycorrhizal fungi Wallander et al. (2001)
Conventional tillage no- Total hyphal length 3.65 and 4.98 m g−1 AM fungi Curaqueo et al. (2010)
tillage (NT)
Cover crops AMF hyphal density 10–35 m g−1 Zea mays + Cover crop Kabir and Koide (2002)
Tillage Management GRSP 45% higher concentration of Zea mays L. Wright et al. (1999)
GRSP in NT than PT
Prairie (Pr) and pasture (Pt) ERH ERH dry weights of 457 and Glomales Miller et al. (1995)
communities 339 µg cm−3 of soil Pr&Pt
communities
Sand dunes AMF biomass AM fungi constituted ~ 30% Glomusintraradices, G. Olsson and Wilhelmsson
of the total microbial claroideum (2000)
biomass
Long-term P exp ERM and IRM ERM was about 10 times Linseed Olsson et al. (1999)
higher biomass than IRM
as largest fraction of SMB
Sterile culture exp AMF mycelia biomass Biomass of internal and Gigaspora margarita Fujiyoshi et al. (2000)
external mycelia of AMF
accounted for ~ 16 and 92%
of root biomass, respec-
tively

GRSP glomalin-related soil protein, EM extrametrical, ERH extraradical hyphal, IRM intra-radical mycelia, PT plow tillage, NT no tillage, SMB
soil microbial biomass

Glomalin‑related soil protein (GRSP)
Other than ERH, AMF also produce hyphal exudates as
glycoprotein-like substance named GRSP with a higher
residence time of 6–42 years in soils (Rillig et al. 2001).
GRSP as carbohydrate chains of asparagine (Wright et al.
1998; Wang et al. 2015) consisting of amino acids, organic
matter, aliphatic compounds viz., methines, methylenes
(Rillig et al. 2003) with auto-fluorescent compound has
received much attention for improving the soil fertility (Wu
et al. 2017), aggregation (Rillig et al. 2002) and as a metal
binding agent (Wright et al. 1996). It might be significantly
larger than SMB carbon as it represents ~ 4–5% of total soil
carbon under tropical forest soil (Miller et al. 1995). GRSP
contributes 20 times more in SOC than microbial biomass
carbon (Rillig et al. 2001). This suggests for the recalci-
trant nature of GRSP which could be ascribed to the high
aromatic carbon therein. (Schindler et al. 2007). In addi-
tion to C sequestration attributed to its measurable propor-
tion and greater residence time in soil, GRSP influence C
storage indirectly by stabilizing soil aggregates. Recently,
Zhang et al. (2017) found that GRSP have much higher
recalcitrance index than SOC and favour C sequestration
either directly by the amount of C retained or indirectly due
to recalcitrant nature. In another study, Wang et al. (2017)
reported greater contribution of GRSP in carbon seques-
tration occuring in deeper soil layers which could be bet-
ter explained in terms of spatial dissociation of SOM, soil
microbes and extracellular enzymatic activity with poor
fresh organic carbon as a source of energy for soil microbes
therein.
Soil aggregation
AMF hyphae and its production of glycoprotein, i.e. GRSP
are indispensable for the formation of soil aggregates. The
development of soil aggregation can be explained by ‘sticky-
string-bag’ mechanism, where fungal hyphae entangle and
enmesh the soil particle and reduce the degradation of the
carbonaceous compound by forming macroaggregates
(Rillig 2004). Soil aggregation provides physical protection
to the large hyphal biomass which otherwise would respire
back to the atmosphere and reverse the C sequestration pro-
cess. Similarly, a close correlation between GRSP, hyphal

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length and aggregate stability was reported by Wright and
Upadhyaya (1996), and they found that greater the aggregate
stabilization, higher will be the C storage in soil. Moreo-
ver, the comparative effects of plant cover, root weight and
length, AMF hyphal length and GRSP concentrations on
soil aggregation of 1–2-mm size class of aggregates were
assessed by Rillig et al. (2002) and they found that the direct
effect of GRSP was much more pronounced than the indirect
effect of AMF hyphae and suggested the hypha-mediated
mechanism of soil aggregate stabilization.. However, the
relationship between hyphal turnover and GRSP content
and their influence on soil stabilizing mechanism still needs
to be addressed.
Plant community
AM fungi have the potential to determine the plant diversity
and their community structure (Hartnett and Wilson 1999;
van der Heijden et al. 1998) by regulating nutrient supply
to them. However, the degree of response by host plant may
vary according to AMF species because C cost and func-
tional benefits are not equally shared between plants (Hart-
nett and Wilson 2002) and further, some plants exclusively
depend on AM fungi for C (Leake et al. 2004) which is
further described in next section.
Recently, the response of AMF under coalfields was
found to be beneficial by promoting plant growth in addition
to higher C storage in soil (Wang et al. 2016). In addition,
van der Heijden et al. (1998) also observed that plant com-
munity diversity and productivity was strongly and posi-
tively influenced by AMF diversity under P limited condi-
tion. Several studies provide direct evidence of changes in
ecosystem processes by changing plant species composition,
and the most dominant process among these is primary pro-
ductivity (Pfisterer and Schmid 2002; Wardle 2002) which is
interlinked with all other processes. However, empirical evi-
dence to support AMF-mediated changes in plant commu-
nity is limited and sometimes may be complex to predict the
response of single plants in a community (Rillig and Rillig
2004). For example, symbiosis loss of highly mycorrhizal
dependent dominated host plant in the community provides
an opportunity to subordinate to release competitively, while
on the other hand AMF also influences competitive interac-
tion even without any involvement with host plants (Marler
et al. 1999).
Plant community and mycoheterotrophy
Merckx et al. (2013) revealed that almost 230 species of
angiosperm are fully mycoheterotrophic and found them
completely dependent on AM fungi for their C demand.
Overall ~ 23,000 species of land plants are expected to rely
on fungi for their C demand at some stage of their life.
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Mycoheterotrophy is the ability of achlorophyllous plants
to obtain the C from mycorrhizal fungi which is associated
with nearby autotrophic plants (Leake 1994). The enrich-
ment of C and N isotope signature study revealed that most
of mycoheterotrophic plants are associated with AM fungi
(Merckx et al. 2010; Gomes et al. 2020) and half of the
AM fungi plants which considered as fully photoautotrophic
could obtain their C from fungi (Smith and Smith 1997;
Dickson et al. 2007). The later source is consistent with
the paris-type AM which is particularly relevant under low
light conditions (Dickson et al. 2007). All AM mycohet-
erotrophs studied till now showed the Paris-morphotype
which is required for fungus to plant C flux (Imhof et al.
2013). The other extensively studied Arum type colonization
which is branched structure develops in cortical cell (arbus-
cules) with intercellular hyphae and present commonly in
crop plants (Gallaud 1905; Dickson et al. 2007). However,
both types of colonization are found in 1:1 distribution in
nature with almost equal frequency (Dickson et al. 2007).
Giesemann et al. (2020) on the basis of stable isotope com-
position of Paris quadrifolia and Arum maculatum observed
that P. quadrifolia contain 50% C of fungal origin while A.
maculatum completely by photoassimilation. Further they
revealed that fungus originated C in P. quadrifolia must
have been received from Arum-morphotype found within a
donor plant. The C flux from Arum to Paris type potentially
could be considered as important development for coherence
in plant community. The C and nutrient transport ability
through mycorrhizal network to mycoheterotrophic plants
is an important feature to shape the species composition
of natural communities as without such association these
mycoheterotrophic plants fail to germinate and no longer
will exist in nature (McKendrick et al. 2000, 2002).
Plant physiology
The role of AMF in better plant nutrition and stress manage-
ment is well understood attributing to greater plant growth
and net primary production. Primary production is critical
for the sequestration of C in soil and their accumulation is
regulated by microbial mediated mineralization and immo-
bilization process. AMF influence both above- and below-
ground C assimilation process by improving plant growth
under various fertility regimes (Kothari et al. 1990; Sub-
ramanian et al. 2008). Furthermore, AMF works as a regu-
latory body to manage photosynthetic activity in a plant,
whereas its activities in plant roots are directly related to net
carbon gain by the host. Some studies suggested that AMF
activity remain unaffected under elevated C ­ O2 concentra-
tion and represent give and take balance between plant and
fungus. However, it has been difficult to prove that whether
increased C gain is directly due to AMF colonization or indi-
rectly due to greater leaf P concentration that accompanies
Archives of Microbiology (2020) 202:1581–1596 1587
fungal colonization (Graham 2000). Wang et  al. (2016)
confirmed greater C storage in coalfield soils as a result
of AMF-mediated improvement in leaf area, chlorophyll
content and the respiratory quotient (Q10 value). Further,
AMF-colonized plants modify their physiological activity
and produce larger above- (Subramanian et al. 2008) and
belowground biomass with highly branched root system
(Kothari et al. 1990) which caused greater C accumulation
in the soil system.
AMF‑mediated C sequestration under future
conditions
Under elevated ­CO2
According to an estimate, in near future, atmospheric C ­ O2
will increase form 20 to > 200% compared to present level
(Pachauri and Reisinger 2007) and in this situation, it would
be interesting to study the plant–fungal interaction and its
influence on C sequestration process. Some evidence sug-
gest that AM fungi are capable to buffer the atmospheric
­CO2 rises with enhanced plant growth and stimulating soil
carbon pool (Wilson et al. 2009; Antoninka et al. 2011).
Contrastingly, Cheng et al. (2012) have presented evidence
that greater plant C allocation to AMF under elevated C ­ O2
Fig. 2  Schematic diagram representing two different pathways under
elevated ­CO2 conditions where cycle 1 is showing that under higher
AMF root colonization plant invests more C into soil via AMF
hyphae to optimize their ­NH4+ demand. Higher labile C in soil stim-
ulates resident soil saprotrophic microbes which results in greater
organic matter decomposition and subsequent release of N ­ H4+ ion.
­(eCO2) enhanced belowground C turnover activity and
respired back this extra soil carbon to the atmosphere. Fur-
ther, they explained that under e­ CO2, plant invests more C
in obtaining soil N as ­NH4+ which otherwise used by soil
nitrifiers (Fig. 2). AM fungi, due to their thinner and longer
hyphae than roots, can exploit more ­NH4+ and deliver it to
host plant with minimum C loss (Govindarajulu et al. 2005).
But to get higher N, AMF may stimulate saprotrophs by
releasing labile C in a low amount which in result allows the
activated saprotrophs to degrade other SOM (Hodge et al.
2001; Drigo et al. 2010). Cheng et al. (2012) also suggest
that under e­ CO2, form of N rather than total N content sig-
nificantly regulates the belowground C decomposition and
plant N acquisition. Therefore, under future environmental
­CO2 conditions, management of N transformation must be
taken into consideration along with terrestrial C cycling.
Nutrient regulation by AMF for other microbes is believed
to be a plausible mechanism to restrict the respiration losses
from stable and labile C pools and greater C retention in soil
(Bradford et al. 2008; Nottingham et al. 2015). Therefore,
Kowalchuk (2012) has provided a conceptual framework
to understand the result of the possible interaction between
AMF and soil saprotrophs on C sequestration under a set of
conditions. According to this framework, poor AMF asso-
ciation with poorly stimulated soil saprotrophs is the best
scenario for net C sequestration point of view.
AMF-mediated pathway of ­NH4+ uptake and their finer hyphae com-
pete with soil nitrifiers for N substrate. In another situation (cycle 2)
low AMF colonization and lower availability of labile C keep resident
soil saprotrophic microbes less active and protect SOM with higher C
sequestration and also exhibit higher nitrifier activity
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1588
However, evidence suggests that higher decomposition
of organic matter performed by AMF under elevated ­CO2
condition is found only under short term while in long term,
they accumulate organic matter due to gain in recalcitrant
compound (Verbruggen et al. 2012). Actually pulse/sud-
den increase in ­CO2 or N may not represent the systematic
and contingent enhancement in nutrient (C and N) leading
to increased decomposition rate. Under long-term situa-
tion, priming of decomposers by AMF disappears as ­CO2
increases gradually (Klironomos et al. 2005). In addition
to this, under permanently shift, altered amounts of inputs
may also bring change in plant litter quality. To quantify the
actual magnitude of priming effect of ­eCO2, indirect effects
of litter quality must also be taken into account to under-
stand the AMF role in contribution of plant-originated soil
C amount. Moreover, under ­CO2 and N enrichment, mycor-
rhizal community structure could also have important influ-
ence on carbon dynamics. For instance, mycorrhizal spe-
cies of Scutellospora and Acaulospora proliferate in better
way under ­eCO2 and Glomus under N-enriched condition
(Klironomos et al. 1998; Eom et al. 1999). In some stud-
ies, greater variations were noticed in quality of mycorrhi-
zal tissue with change in genera and species which further
casted significant influence on C cycling. However, more
extensive studies are required to broaden our knowledge to
understand the difference in quality and physiology of AMF
tissue among various groups in order to predict their effects
on C dynamics.
Under elevated ­CO2 and temperature
Global rise in C
­ O2 level is closely interlinked with increment
in temperature which results in global warming. According
to an estimate by 2100, ­CO2 level will reach to 1000 ppm
which would increase air temperature by 4 ℃ than pre indus-
trial level (IPCC 2014). Temperature influences the AM
fungi directly or indirectly via effecting host plant growth,
physiology, resource-demand and soil nutrient availability.
Mohan et al. (2014) summarized the warming effect on AM
fungi and concluded that mycorrhizal abundance increases
in 63%, decreases in 17% and exhibited neutral or non-sig-
nificant response in 20% studies with rising temperature.
AM fungi-mediated soil C regulation is still unclear and
their role in managing the soil C balance is significant with
changing temperature. Increased temperature affects the C
allocation to fungi which, in turn, either enhances the C
respiration (Hawkes et al. 2008) or improves the soil C stor-
age via down regulation of respiration or by increasing the
biomass of fungal mycelium (Heinemeyer et al. 2006). How-
ever, raising temperature may enhance the C distribution to
AM fungi, P acquisition and root colonization rate (Kytoviita
and Ruotsalainen 2007). In addition to AM fungi, increased
temperature can also influence the morphology and lifespan
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Archives of Microbiology (2020) 202:1581–1596
of root biomass which subsequently affects the C balance in
soil (Norby and Jackson 2000). In temperate region, incre-
ment in net primary productivity with increasing tempera-
ture is obvious due to longer growing period which results
in more C allocation to AM fungi with greater plant biomass
accumulation, as depicted in Table 3 and Fig. 3 (van Wijk
et al. 2004). Concomitant variation in temperature and other
factors or drivers can influence the ecosystem process by
regulating the plant-mycrorrhizal symbiosis. For example,
in tundra region in Abisko, AM colonization in dwarf shrub
decreased with rising temperature and this effect was more
pronounced when warming and ­CO2 combined together
(Olsrud et al. 2010). Contrastingly, Vicca et al. (2009) in
their study found that combined warming and C ­ O2 enrich-
ment increased mycorrhizal colonization and reduced the
stimulation of soil respiration. However, data related to
combined effect of elevated C ­ O2 and temperature on AM
fungi-mediated C cycling are scarce which require multi-
factorial approaches with multi-disciplinary research and
long-term field manipulations to improve our understanding
how global climate change influence the plant-mycorrhizal
symbiosis and related ecosystem functions.
Modification in source–sink relationship
under changing climate
AMF remain entirely dependent on plants for their car-
bon demand and it has been reported that AMF used 4.3%
of recently plant fixed C within single day (Tome et al.
2015). Sometime this demand is high enough to supress
the early plant growth (Jakobsen 1999; Graham 2000; Ryan
and Graham 2002). However, it is also hypothesized that
AMF create C sink strength and maintain the higher pho-
tosynthetic rate by regulating the product feedback inhibi-
tion mechanism and compensate the plant C use by AM
fungi (Kaschuk et al. 2009; Schweiger et al. 2014). This
source–sink interplay in plant-mycorrhizal symbiosis will
significantly influence C fixation through photosynthesis and
its belowground availability under future climatic conditions
(Fatichi et al. 2014; Finzi et al. 2015). However, earlier it
was uncertain whether enhanced C assimilation in mycor-
rhizal plants is due to greater nutrient supply or downward
C flow to mycorrhizal roots or by other alternative mecha-
nism. Regarding this, Schweiger et al. (2014) reported that
considerable extent of metabolic changes (at least 50%) and
higher C assimilation in mycorrhizal Plantago major were
independent to nutrient availability (P concentration). For
more clarification, an alternative mechanism was suggested
that higher gas exchange and source sink interplay in plant-
mycorrhizal symbiosis could be due to aboveground source
to above or below ground sink (Godbold et al. 2006; Moyano
et al. 2007; Kaschuk et al. 2009). However, such hypoth-
eses were not experimentally supported and regarding this
 Table 3  Carbon sequestration by AMF under various management conditions
Crop (cultivar) Agro ecology/contaminate site AMF Effect on carbon pool References
Active pool Passive pool

Cereal-legume Long-term fert. exp + Bio-C ↑ 38%, WSC ↑ 20.8 HWSC ↑ GRSP ↑ 33%, SOC ↑ 6.3% in AMF (+) Subramanian et al. (2019)
9.3% in AMF (+) over control over C and ↑ significantly (p ≤ 0.05) ↑
both HA and FA fractions
Archives of Microbiology (2020) 202:1581–1596

Wild cherry, Cerasushumilis
Yellow horn and apricot
Maize (Zea mays L.)
Metrosiderospolymorpha
N/A
Sophoraviciifolia
Grassland, forest and arable land High-elevation Tibetan ecosyst
Poplar forest
Long-term meadow
Plantagolanceolata
Coalfields + N/A SOC ↑ 52–61% and EE-GRSP and Wang et al. (2016)
T-GRSP ↑ 55–70 and 36–44% respec-
tively in AMF (+)
Pot exp + WSC ↑16.1–116.1% POM ↑25–200% in SOC ↑3.7–23.3 and HA and FA ↑ Srimathi et al. (2014)
AMF (+) over control 25–283 and 50–191% resp. while
T-GRSP and EE-GRSP ↑210–520 and
63.6–163.65% resp. in AMF (+) over
control
Tropical forest N/A Soil microbial Bio-C constituted 0.08– GRSP accounted as 4–5% of total soil C Rillig et al. (2001)
0.2% of total C
eCO2 @380 and 580 (ppmv) + N/A AMF ↓ SOC by 9% and total C by 15% Cheng et al. (2012)
Heavy metal cont. site N/A N/A SOC was sig. correlated with T-GRSP Yang et al. (2017)
(0.48–0.61) and EE-GRSP (0.39–0.57)
under various depth
+ AMF in forest and grassland were positively related to EE-GRSP, T-GRSP, SOC, Xu et al. (2017)
unprotected and physically protected C fractions, but not in arable land
eCO2 @380 and 580 (ppmv) + Fungal ERM not influenced by elevated C ­ O2 but ERM may play significant role in Godbold et al. (2006)
transfer of root-derived C to SOM
Field incubation and glasshouse Exp + Presence of AMF suppressed the decomposing saprobes; AM fungi may contribute Verbruggen et al. (2016)
positively to C persistence in soil
14.2–26.1 °C temp + As climate warms, less soil C storage by AMF due to higher fungal respiration Hawkes et al. (2008)
Microcosm study

WSC water soluble carbon, POM particulate organic matter, T-GRSP total-glomalin related soil protein, EE-GRSP easily extractable glomalin-related soil protein, ↑-increases; ↓-decreases; Bio-
C biomass carbon, HWSC hot water soluble carbon, HA humic acid, FA fulvic acid

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1590 Archives of Microbiology (2020) 202:1581–1596

Fig. 3  Conceptual framework
is illustrating that AMF fungi
under elevated C ­ O2 conditions
demand for higher photosyn-
thetic fixed C as a result of
higher net primary productiv-
ity (NPP). This additional C
remains in the soil as hyphal
biomass, root exudates or
hyphal exudates, i.e. GRSP.
Larger hyphal biomass due
to the presence of chitin-
ous cell wall and recalcitrant
nature of GRSP increases the
accumulation of C in soil with
greater stability. In addition,
hyphal biomass and GRSP also
improve aggregate stability and
further reduce SOM decomposi-
tion

Kaschuk et al. (2009) emphasized on experimental evalu-
ation of mycorrhizal C sink strength and its effect on soil
C storage which is having potential from environmental
perspective. Recently, a lab experiment revealed that reduc-
tion in sink strength by excision of extraradical mycelium
of AM fungi in cucumber roots reduced the photosynthetic
rate by 10–40% while under ­eCO2 (700 ppm) this effect was
found minor (Gavito et al. 2019). This direct experimental
evidence of sink strength as influenced by AM fungi on pho-
tosynthesis potential has great implication in designing the
adaptation trial of agricultural crops under future climatic
conditions. In addition, such study further increases our
knowledge regarding modelling response in elevated C ­ O2
and soil C sequestration.
Factor affecting C turnover in AMF
Soil environment
AMF hyphae by soil fauna due to greater physical protection
offered by soil system. In addition to this, a short incuba-
tion study (De Vries et al. 2009) revealed that a fraction of
fine AMF hyphae and saprophytic fungi were most sensi-
tive towards fertilization and disturbance with short turno-
ver period while another fraction composed of saprotrophic
fungi and runner hyphae of AMF was influenced less by
fertilization and disturbance with higher turnover period.
In other factors, soil moisture dictates the AMF mycelium
turnover rate possibly by lower decomposition under drought
condition and shapes the standing crop of hyphae in soil
system (McHugh and Schwartz 2015). Soil disturbance and
quality of litter may also influence AMF abundance and sub-
sequent organic matter decomposition rate through affecting
saprobes’ activity. Verbruggen et al. (2016) found that dis-
turbance caused by the rotation of cores is directly respon-
sible for higher OM turnover and saprobe abundance while
the presence of fresh organic matter caused suppression of
saprobes by AMF to take advantage of newly added litter.

Soils as a complex system are having diverse physical,
chemical and biological properties which influence AMF
community structure and their decomposition. In a study
conducted by Staddon et al. (2003), it was reported that AM
fungal hyphae network had very limited turn over period
and is respired back to the atmosphere within a short time
period. However, semi-sterile conditions of the experimental
growth medium devoid of soil biota might have resulted in
the lower turnover period which otherwise is enhanced due
to grazing nature of soil fauna. Similarly, Zhu and Miller
(2003) have also pointed out the lower decomposition of
AMF composition and hyphal characteristics
Glomeromycota includes ~ 270 species of AMF (Goto et al.
2012; Marinho et al. 2014; Oehl et al. 2015) with large func-
tional diversity (Maherali and Klironomos 2007). AMF spe-
cies diversity is vulnerable to anthropogenic changes (Oehl
et al. 2010; Verbruggen et al. 2010) and these changes may
affect their ecological function. Xu et al. (2017) opined that
long-term cultivation or changes in land use management
might result in alteration or permanent losses of some spe-
cific AMF taxa with greater C losses which could not be

13
Archives of Microbiology (2020) 202:1581–1596 1591
easily compensated and hence the need to implement some
more effective interventions. In addition to this, Treseder
and Allen (2000) predicted that shifts in the AMF commu-
nity might lead to some important and significant influence
on mycorrhizal C dynamics. For example, Scutellospora and
Acaulospora species prefer to proliferate under elevated ­CO2
while Glomus remains dominant under N deposition (Kli-
ronomos et al. 1998; Egerton-Warburton and Allen 2000).
Regarding hyphal characteristics, the obligate nature of
AMF restricts our knowledge about their chemical com-
position and growth morphologies. Some species differ
in their GRSP production ability (Gigaspora and Glomus
produce approx. 20 and 60 µg protein m ­ g−1 hyphae, respec-
tively) with thicker walled hyphae containing higher chitin
providing greater resistance to decomposition (Wright and
Upadhyaya 1996). GRSP as glue-like substance stabilize the
soil aggregates and provides greater physical protection to
AMF hyphae. The presence of intra radical hyphae in fine
roots delays the decomposition of the latter due to chitin-
ous nature of hyphae wall (Frey et al. 1994; Langley and
Hungate 2003). Further, Staddon et al. (2003) on the basis
of hyphal architecture purposed two pools: one is known as
absorptive or exploratory hyphae with fast turnover rate, and
another is composed of thicker walls with arterial architec-
ture and slow turnover rate. The absorptive or exploratory
hyphae leave resistant chitin (Staddon et al. 2003) and GRSP
(Wright and Upadhyaya 1998) after their rapid turnover and
contribute in soil stable C pool (Rillig et al. 2001).
Elevated atmospheric ­CO2
The effect of elevated ­CO2 on AMF hyphae turnover is
quite limited and contrasting as reported in various stud-
ies. In a study, Godbold et al. (2006) found little effect of
elevated ­CO2 on soil carbon input through hyphal turnover
while elevated ­CO2 itself increased soil C inputs through fine
roots’ decomposition. Similarly, Treseder and Allen (2000)
reported both increased and minute effects of elevated C ­ O2
on AMF hyphal biomass and theses responses have been
proved to be species-specific (Kubiske and Godbold 2001).
However, the response of ERM biomass to elevated ­CO2
might also be explained by dominated host plants (Fitter
et al. 2004). Overall, the production of large biomass of
AMF hyphae and high turnover rate potentially add them
into the pool of soil C. Further, a study on grassland commu-
nity revealed that elevated C­ O2 level and temperature stimu-
lated respiration on pasture soil with mostly sequestered C
belowground, exhibit respiration as an important integral
of carbon balance (Friedlingstein et al. 2006; Bahn et al.
2008). In contrast, as earlier explained, ­CO2 enhancement
of AMF influences soil saprotrophs microbial community
which results in greater C losses from the soil system (Cheng
et al. 2012).
Interaction of AMF × soil microbes
The AMF may affect the soil C by influencing decompo-
sition rate of SOM through interaction with another soil
biota. However, AMF is not directly involved in organic
matter decomposition but remain dependent on saprophytic
microbes for nitrogen availability through decay of complex
carbon sources. Hodge et al. (2001) reported higher miner-
alization rate in the presence of AMF without producing
enzyme required for the organic matter break down. The
possible interaction between AM fungi and other microbes
including saprophytic could be due to rhizodeposition of
hyphal exudates. In addition, Leigh et al. (2011) reported
antagonistic interaction between saprophytic bacteria and
AM fungi which suggested competition for decomposed
products. However, in a study (Walley et al. 2014) co-inoc-
ulation of AMF and plant growth promoting rhizobacteria
(PGPR) could not enhance the bulk soil C and N signifi-
cantly beyond what could be achieved by sole organism and
also revealed that GRSP is either not exclusive to AMF ori-
gin or represent only a small fraction of total soil protein.
The C uptake and allocation as the function of source-sink
relationship, starch mobilization and leaf P concentration
were studied in soybean (Harris et al. 1985) and found that
mycorrhizal inoculation enhanced photosynthate to 12% in
root nodule with 52% higher ­CO2 fixation in plants leaf com-
pared to without microbial symbionts. Apart from indirect
effect, mycorrhizal fungi as an important dietary source of
micro (Ruess et al. 2000) and meso fauna (Ngosong et al.
2014; Kanters et al. 2015) in the belowground food web,
influence mycelium turnover in soil. Interestingly, soil fauna
exhibits preferential grazing behaviour
toward some specific mycorrhizal fungi (Maraun et al.
2003) which either reduces or eliminated certain taxa from
the bulk mycorrhizal community and ultimately affects soil
C storage (Clemmensen et al. 2015).
Future prospects
Now, it is evident that AMF are important in global C cycling
regulating the delivery and flux of C in soil. However, the
potential effect of AMF on C sequestration or decomposition
varies considerably. AMF fungi mostly contribute to soil C
via their hyphae and glycoprotein, i.e. GRSP. The higher
contribution of AMF hyphal biomass in C sequestration
can be explained due to larger amount of residual portion
remaining after decomposition and presence of chitinous
cell wall of recalcitrant nature. Though overall SOM stor-
age depends on hyphal architecture, GRSP production and
aggregate stability, it still needs to be considered and stud-
ied further. Second, soil C cycle is closely inter linked with
the N cycle, and it must be taken into account for a better
13

1592
understanding of C flux in soil–plant atmosphere contin-
uum. More specifically, our future research efforts must be
focused on nutrient form rather than the total quantity avail-
able to plant because Cheng et al. (2012) pointed out that
the plant translocates more C to belowground in response
to higher N­ H4+ concentration, not the N­ O3− as available by
AMF, which may enhance C turnover compared to storage
in soil. Other than nitrogen, soil phosphorus response is well
established on AMF diversity and abundance, but their role
in AMF-mediated C cycling is uncertain and requires further
study. Recently, AMF association with other soil microbes
received much attention to explain their interaction effect
on soil C turnover. However, large contradictions in the
results require following the mechanistic understanding of C
turnover and its response under changing climatic and land
use management practices. Last, we have to focus more on
long-term studies which consider total gain via plant growth
promotion effects, soil aggregation, recalcitrant mycelium
products and priming effects on decomposer to predict the
actual effect of changing climate on C sequestration poten-
tial of AMF.
Compliance with ethical standards  Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lin-
Conflict of interest  The authors declare that they have no conflict of
interest.
Ethical approval  No studies with humans/animals have been performed
by any of the authors for the purpose of this review article.
Informed consent  Informed consent was taken from all the authors.
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