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Mycorrhizal-induced growth depression in plants
Liang Jin
1
&Qian Wang
2
&Qiang Wang
2
&Xiaojuan Wang
1
&Alan C. Gange
3
Received: 18 January 2016 /Accepted: 4 September 2016 /Published online: 15 September 2016
#Springer Science+Business Media Dordrecht 2016
Abstract As plant mutualists, one would not expect
arbuscular mycorrhizal fungi (AMF) to cause growth depres-
sion of their host plants. The mechanism responsible for neg-
ative effects of AMF is still debated and so here we review the
possible abiotic and biotic reasons for AMF-induced growth
depression in plants: 1) The Phytocentric explanations, in-
clude: a) AMF and non-mycotrophic plants, b) different
growth stages of plants. 2) The Mycocentric explanations,
include: a) Low effective AMF species, b) The existence of
vesicles, c) Genetic variability of AMF, and d) Geographic
origin of AMF. 3) Unbalanced C-for-nutrient-trade, involving
both partners and 4) Indirect effects of other organisms. We
note deficiencies in previous studies and suggest improve-
ments in experimental designs such as the use of realistic
mixtures of AM fungal species, and growing plants in mix-
tures in field situations, rather than single pot studies, with and
without fungi. Determining whether and how AM fungi cheat
on their hosts will enable a better understanding of their roles
in natural communities and their use as biofertilizers in
agriculture.
Keywords Abiotic and biotic stress .Arbuscular mycorrhizal
fungi .Growth depression .Negative effect .Parasite
1 Introduction
Arbuscular mycorrhizal fungi (AMF) comprise one of the
most important groups of micro-organisms in terrestrial
ecosystems, forming a symbiosis with more than 80 %
of vascular plants (Wang and Qiu 2006). It is generally
accepted that AMF are obligate biotrophs and have zero
fitness in the absence of a host plant (Berruti et al. 2016).
With the widely distributed external hyphae, AMF can
increase nutrient acquisition and water absorption (Smith
and Read 2008). They can also alleviate environmental
stresses (Chandrasekaran et al. 2014) and enhance plant
resistance to pests and pathogens (Yang et al. 2014).
Thus, AM symbiotic associations can influence the fitness
of individual plants (Koide and Dickie 2002), the compo-
sition of plant communities (Hartnett and Wilson 2002),
inter-specific competition (Jin et al. 2011), and productiv-
ity within terrestrial ecosystems (Klironomos et al. 2000;
vanderHeijdenetal.2008).
Plants supply AMF with photosynthetic products, while
the fungi enhance the ability of plants to obtain nutrients,
particularly P and N (Treseder 2013; Hodge and Storer
2015). Thus, AMF can enhance the growth and survival of
host plants, as well as increasing biomass production.
However, it is not true that all host plants gain net benefits
from symbiosis with the AMF. Some of the AM fungi cause
negative effects in host plants, such as nutrient outflux
(Mariotte et al. 2013) or growth depression (Graham 2000).
As plant mutualists, this is unexpected and begs the question:
Why do some AMF appear to cheat on their host plants? Janos
(1985,1987,1996) and Smith and Smith (1996) first exam-
ined the potential for parasitism by mycorrhizal fungi in the
context of Bcheating^. Subsequently, Johnson et al. (1997)
and Gange and Ayres (1999) discussed the mutualism-
parasitism continuum, including negative effects of AMF on
*Liang Jin
jinliang@sstm.org.cn
1
Natural History Research Center, Shanghai Natural History Museum,
Shanghai Science & Technology Museum, Shanghai 200127, China
2
State Key Laboratory of Grassland Agro-Ecosystem, School of
Pastoral Agriculture Science and Technology, Lanzhou University,
Lanzhou 730020, China
3
School of Biological Sciences, Royal Holloway, University of
London, Egham, Surrey TW 200EX, UK
Symbiosis (2017) 72:81–88
DOI 10.1007/s13199-016-0444-5
the performance of the host plant. A mechanistic explanation
for the negative effects of AMF on the performance of the host
plant was provided by Smith and Read (2008) and Johnson
(2010), who proposed a trade balance model, further advanced
by the review of Smith and Smith (2011). A recent paper
(Jones et al. 2015) suggests that while there may be evidence
for low-quality partners in mycorrhizal mutualisms, there is
actually little evidence for cheating by the fungi. Yet abundant
theoretical work shows that such negative effects are required
to prevent Robert May’sfamous‘orgy of mutual benefaction’
from occurring (Holland 2015). Here, we explore the mecha-
nisms by which negative effects of mycorrhizas might occur
(and illustrated in Fig. 1), our aim being to suggest a series of
research questions that should address the question as to
whether mycorrhizal fungi can cheat on their partners. It is
generally accepted that plants and AMF symbiotically trade
the commodity that they can most readily procure - plants
trade carbon and fungi trade mineral ions and water. But the
effects of mycorrhizas are far more complex than this, so what
other factors might play a role in cheating?
2 Phytocentric explanations
2.1 AMF and non-mycotrophic plants
In natural ecosystems, there are some non-mycotrophic plants
which do not form a symbiosis with AMF, including species in
the families of Amaranthaceae, Brassicaceae, Caryophyllaceae,
Polygonaceae, Urticaceae, Cyperaceae, Haemodoraceae,
Proteaceae and Restionaceae (Lambers and Teste 2013).
Arabidopsis thaliana is one of these plants in the Brassicaceae.
It has been reported that most of the plants in this family do not
form a symbiosis with AMF (Brundrett 2009). However, Veiga
et al. (2013) found that in some cases, A. thaliana can be colo-
nized with a mycorrhizal species (Rhizophagus irregularis). The
interaction did not bestow positive benefits on A. thaliana,but
hadanegativeinfluence,shownbygrowthdepressioninthe
colonized plants (Veiga et al. 2013). The reason maybe that
when AMF mycelia make contact with the roots of these plants,
costly chemical defences are produced using resources that
might otherwise have been directed to plant growth (Song
et al. 2011). In the case of non-mycotrophic plants, the roots
may perceive a need to defend against the potential colonization,
e.g., by changing morphology for physical protection or produc-
ing secondary metabolic products (e.g. Hetrick et al. 1990;
Vierheilig et al. 1996). Such growth or production requires extra
photosynthetic products and may result in growth depression if
resources are limited. It would be most instructive to pursue
more studies like the one by Veiga et al. (2013) and to challenge
a range of non-mycorrhizal plants with different AM fungi spe-
cies. Metabolomics could then be used to examine the chemical
mechanisms involved.
2.2 Seedling growth stages of plants and competition
Growth depressions may also be seen at different stages in the
life of a plant. Janoušková et al. (2011)showedthat
Fig. 1 Mechanisms of
mycorrhizal-induced growth
depression in plants
82 L. Jin et al.
Tripleurospermum inodorum plants responded positively to
mycorrhiza when grown in a nutrient-deficient soil, the re-
sponses being more significant with P uptake than with nitro-
gen uptake or growth. In contrast, growth of nearby seedlings
of this species and of the non-mycorrhizal Sisymbrium loeselii
was inhibited in the mycorrhizal treatments. Importantly, the
plants were grown in boxes in which seedlings were establish-
ing in soil containing hyphae, but not roots. This suggests that
the growth of the seedlings was depressed by nutrient deple-
tion (particularly P) in the extra radical mycelium radiating
from the large plants (Janoušková et al. 2011). Further evi-
dence for this effect was provided by Del Fabbro and Prati
(2014). These authors found that seedlings of Senecio
inaequidens and S. vernalis were smaller in the presence of
AM hyphae in soil, even though no fungal colonization of the
seedlings could be detected. The results of these studies point
to an important aspect of mycorrhizal effects on the coexis-
tence of large plants and seedlings in nutrient deficient sub-
strata. Similarly, the identity of the nearby large plant is alsoan
important determinant with respect to whether AM fungi may
negatively affect the growth of seedlings. Seedlings can con-
nect to a common mycelial network in the soil and their
growth can be reduced if establishing near an adult plant of
a different species, compared with those that establish near to
a conspecific plant (Burke 2012). This further emphasizes that
future experiments need both to grow plants in mixtures, and
to take account of the identity and ages of plants in those
mixtures too.
Competition between plants is likely to be of paramount
importance in determining the outcome of the interaction be-
tween AMF and the host. For example, Allsopp and Stock
(1992) found that Aspalathus linearis was non-responsive at
low plant density, but negatively responsive to AMF at high
density. The intensity of intra specific competition and the
distribution of plant sizes in populations can be shifted by
AMF, resulting in many small individuals if colonization is
high (Ayres et al. 2006). Interspecific competition is also in-
fluenced by AMF, particularly if competing species differ in
their responsiveness to the fungi (Watkinson and Freckleton
1997). A knowledge of the responsiveness of different crops
and weeds is essential if AMF are to be of use in agricultural
situations (Daisog et al. 2012).
3 Mycocentric explanations
3.1 Low effective AMF species
It is well known that AMF species differ in their ability to be a
‘good’partner for a plant, but quite what constitutes ‘good’or
separating such measurement from environmental influences
presents many challenges (Werner and Kiers 2015). Indeed,
the frequency of poor AM partners may be very hard to
discern in natural communities, when their presence may be
masked by other, more effective fungi (Hart et al. 2013).
These mycorrhizal species may provide no or only a few ben-
efits to the host plant, such as a little P, N nutrients or water,
even though they form mycorrhizal structures within plant
roots. The inefficiency of the fungi may be due to either poor
development of fungal structures or to a lower rate of transfer
per unit area of the symbiotic interface (i.e. flux across the
interface). Hart et al. (2013) reported that there were several
low effective AMF species, including Entrophospora
colombiana,Glomus aggregatum,Glomus etunicatum,
Rhizophagus irregularis (Glomus intraradices)and
Scutellospora calospora. However, the context-dependency
of such interactions is again illustrated by the fact that there
are many reports of R. irregularis conferring beneficial effects
on plants, including increased yield (e.g. Hijri 2016), resis-
tance to pathogens (e.g. Mora-Romero et al. 2015) and toler-
ance to toxic substances, such as arsenic (e.g. Cattani et al.
2015). However, such beneficial effects can also be plant
genotype-specific (Mora-Romero et al. 2015).
It has been demonstrated that low effective AMF are wide-
ly distributed in natural habitats. Increasing the diversity of
plant species could reduce the negative effects on individual
host plants (Hart et al. 2013). Burrows and Pfleger (2002)
found that high diversity of host plants could mitigate the
growth depression of host plants with AMF. When diversity
was high, those species antagonized by AMF were less affect-
ed, implying that mycorrhizal growth responses of individual
plants may not translate to the population or community level.
We again suggest that all future experiments that seek to in-
vestigate fungal partner ‘quality’should take place in realistic
scenarios of plants growing in mixtures (or monocultures for
crops) rather than individuals in pots.
A further problem with the literature is that it is replete with
experiments involving ‘control’(non-mycorrhizal) plants be-
ing compared with inoculated individuals. In many cases, the
latter involves one species of fungus. Yet such scenarios are
most unrealistic, and such controls for the most part inappro-
priate (Partída-Martinez and Heil 2011), because uncolonized
plants are virtually absent in nature, and thus the ‘normal’
ecological outcome of the interaction between AMF and host
plant may be obscured. Such experimental designs are of
course useful when trying to elucidate the interactions be-
tween mycorrhiza and plant at the molecular level, but they
may provide a misleading ecological outcome. Future ecolog-
ical experiments need to involve combinations of fungi, to
determine whether functional redundancy or cheating exists
amongst mycorrhizal species in any particular association
(Treseder et al. 2012). Perhaps of most importance is that
molecular techniques need to be used to quantify the different
fungal species in the roots at the end of such experiments.
Fungal abundance may then be correlated with various host
plant traits, leading to testable hypotheses regarding the roles
AM depress plant growth 83
of the various species (Partída-Martinez and Heil 2011). On
the rare occasions when this has been done (Robinson Boyer
et al. 2015), relative fungal abundance has been shown to be
affected by water availability. It is highly likely that other
environmental parameters, such as nutrients, will similarly
affect the outcomes and could go a long way to explaining
the variable effects seen in previous studies (Table 1).
3.2 The existence of vesicles
Growth depressions may also be attributed to the occurrence
and functioning of the various AM structures. It is remarkable
that even today, the majority of studies express AM
colonization as ‘total percent root length colonized’,giving
little indication of the occurrence of the different kinds of
structures within roots, namely hyphae, arbuscules, vesicles,
and spores. The vesicle is one of the most obvious structures
which can be observed in tissues of plant roots. However, the
function of vesicles is still debated today. There are two opin-
ions about it. One is that vesicles have a propagule function
and can support the regrowth of intercellular hyphae when
appropriate conditions occur (García et al. 2008). More vesi-
cles were formed under stress conditions showing the tenden-
cy of AMF to invest more energy in storage structures for
survival (García et al. 2008). When adverse conditions
prevailed, such as drought stress, salt stress or high tempera-
ture, vesicles could survive in these conditions. After the con-
ditions improved, vesicles could be activated and new fungal
structures could be regenerated. The second opinion is that the
vesicles are purely storage tissue for AMF (Li 2007). No
matter which is correct, it is suggested that the existence of
vesicles may decrease the growth rate of plants (Johnson
1993), through direction of resources to these structures.
Perhaps of more interest is the observation that
R. irregularis (as G. intraradices) reduced the growth of a
non-host plant only when hyphae and vesicles were present
(Wagg et al. 2011). The reason maybe that when vesicles
grow, the fungus needs to obtain more photosynthetic prod-
ucts from the host plant, resulting in plant growth depression.
We suggest that in all future studies that report AM coloniza-
tion of plants, data for the different structures should be in-
cluded. Simply presenting total colonization may hide a lot of
useful and interesting data.
3.3 Genetic variability of AMF
Variation in the outcome of mycorrhizal colonization of plants
may be partially based on fungal genetic variability and there
can be high rates of genetic variability in AMF populations
(Koch et al. 2004). Koch et al. (2006) found that different
AMF isolates exhibited different influences on host plants
even though they belonged to the same species
(R. irregularis (G. intraradices)): some of them promoted
the growth of host plants, and some of them decreased growth.
This means that genetic variability in an AMF population can
cause a range of different outcomes of plant growth, which
could also be ecologically relevant at the ecosystem level and
be important for the development of potent AMF inocula as
successful biofertilizers (Rouphael et al. 2015). Such variabil-
ity was further emphasized by de Novais et al. (2014)who
Tabl e 1 Results of the relationship between AM fungi and C-for-nutrient trade for host plant
Plant AM fungi Nutrients Effects of AM on plant Reference
Vetiveria zizanioides Acaulospora scrobiculata,
Glomus aggregatum,
Glomus sp.
No P-supplied, + Techapinyawat et al. 2002
30, 60, 90 kg P
2
O
5
/ha −or 0
Macaranga
denticulata
Glomus spp., Glomus
fasciculatum,
Acaulospora spp.
Low P + Youpensuk et al. 2005
High P (25–150 mg P/kg soil) −or 0
Oryza sativa Rhizophagus irregularis,
Funneliformis mosseae
Limiting N (0.15, 0.23, 0.45,0.79 mM
(NH
4
)
2
SO
4
+ Correa et al. 2014
High N (1.88, 3 mM (NH
4
)
2
SO
4
)−or 0
Wheat Paraglomus sp., Glomus sp. Conventional production + Dai et al. 2014
Organic production −
Oryza sativa Glomus mosseae Low N level (20 mg pot
−1
) More positive effects from
AM to plant in low N than
high N level
Liu et al. 2013
High N level (50 mg pot
−1
)
Wheat (Triti cu m
aestivum)
Funneliformis ssp.,
Rhizophagus ssp.,
Claroideoglomu ssp.
Adverse soil condition More benefits under adverse
soil condition than
favourable soil conditions
Aghili et al. 2014
Favourable soil conditions
B+^means positive effects, B−^means negative effects, B0^means neutral effects
84 L. Jin et al.
demonstrated that 41 AMF-plant combinations had responses
ranging from functionally compatible interactions to essential-
ly neutral with their host plants. Furthermore, Klironomos
(2003) also found that plant growth responses to different
AMF inoculation within an ecosystem can range from highly
parasitic to highly mutualistic. Clearly, genetic variability of
AM fungi is very important in determining the outcome of the
interaction with the host. Indeed, this may be as important as
fungal phylogeny itself. However, relatively few studies have
explored the importance of fungal phylogenetic effects on
growth depressions in plants (but see Mummey et al. 2009).
It would be instructive to examine the role that phylogeny
plays in AMF-induced plant growth depression, particularly
as plants in natural communities tend to be associated with a
variety of fungal species (Davison et al. 2011).
3.4 Geographic origin of AMF
That populations of AMF from different geographic areas vary
genetically has been known for some time (Giovannetti et al.
2003). Indeed, Mummey et al. (2009) show that growth de-
pressions in plants may occur depending on the geographic
origin of the fungus. Other good examples of this type of
problem come from trials of commercial inoculants, not all
of which are successful, and which often produce undesirable
effects (Herrmann and Lesueur 2013). For example, Williams
et al. (2013) found that commercial inoculation with AMF did
not increase the growth of Podocarpus cunninghamii, but in-
steadcausedgrowthdepressionanddecreasedPandN
concentrations in plant tissues. Furthermore, Faye et al.
(2013) found that only three out of 12 different commercial
inoculants had a beneficial effect on growth of maize. The
reason maybe that although there is little significant specificity
in the relationship between AMF and their host plants, local
adaptation occurs, whereby plants may select the most benefi-
cial partners (Werner and Kiers 2015). Because most native
AMF have co-evolved with their host plant in any given areas,
they may have a closer relationship with each other, than com-
binations that are geographically isolated. These interactions
are most likely driven by variation in local resources, primarily
soil fertility (Johnson et al. 2010). To date there are relatively
few studies that have investigated the consequence of AM
geographic origin on host plant performance, and this would
be another fruitful area for research. One example is that of
Antunes et al. (2011), in which six AMF species were collected
from cool and warm climatic conditions and used to colonize
cool-adapted Poa pratensis and warm-adapted Cynodon
dactylon grasses. With P. pratenis, five (83 %) of the cool-
adapted fungi in warm conditions resulted in growth depres-
sion, while with C. dactylon, four (67 %) warm-adapted fungi
produced growth depressions in cool conditions. This clearly
shows how abiotic conditions, such as climate and ecotype
variability of the fungi, can interact to affect plant growth.
Such problems with geographic origin or genetic variation
in AMF may well be why these fungi have yet to realise their
potential as biofertilizers (Herrmann and Lesueur 2013,but
seealsoRouphaeletal.2015). A better understanding of how
and why AMF may cause growth depressions in plants would
enable the production of inocula that can be used in a wide
variety of agricultural or horticultural situations.
4 Unbalanced C-for-nutrient-trade
C-for-nutrient trade is certainly the most obvious key factor in
predicting the outcome of AMF symbioses. It has long been
known that AM benefits to plant growth tend to be lower
when soil P is high (e.g. McArthur and Knowles 1992)and
similar effects seem to hold true for soil N (Correa et al. 2014)
(Table 1). It is now becoming clear that the ‘cost/benefit’
approach is more complex than previously thought.
Hoeksema et al. (2010) and Werner and Kiers (2015)pointed
out that AMF-host plant relations are context-dependent and
can be mediated by abiotic factors, including soil nutrients,
pH, water and sunlight. Light availability (i.e. photosynthetic
activity) has long been thought to be the limiting factor of
symbiont activity and plant growth (Reinhard et al. 1993),
though this is not always so and is dependent upon plant
identity (Stonor et al. 2014). Carbon cost analyses of plants
suggest that the effectiveness of AMF ranges from mutualistic
to parasitic depending mostly on soil nutrient supply in natural
or artificial ecosystems. It is clear that future studies of the
effects of AMF on plants should take place along gradients
of soil nutrients and that current levels of knowledge regard-
ing C/N dynamics in particular are poor (Correa et al. 2015).
Yet, a remarkable amount of the literature has involved exper-
iments that have not varied the soil nutrients, even though
natural soil levels are known to be extremely heterogeneous.
Growth depressions may be caused by AM fungi when the
demands for organic carbon (C) from the host plant outweigh
any benefits which might be produced from phosphorus or
nitrogen transfer via the common mycelial network
(Table 1). In this way, the mycorrhiza is essentially acting as
aparasiteora‘cheater’(Johnson et al. 1997). However, the
situation is complicated greatly by there being much variation
in the ‘quality’of the fungal partners and the degree to which
plants can control the carbon outflow to the mycorrhiza
(Grman 2012; Werner and Kiers 2015). It is also quite possible
to observe a positive or negative effect of colonization of a
plant by a fungal species (or combination), depending on the
prevailing environmental conditions and fungal abundance
(Gange and Ayres 1999). There is a real need to use molecular
techniques that quantify the amount and metabolic activity of
each fungal species over time in root systems during experi-
ments, and to relate their presence to growth effects in the
plant, linked with measurements of nutrient inflows and
AM depress plant growth 85
carbon outflows (Thonar et al. 2012). A good example of
the latter, in a controlled experiment, is the study by
Robinson Boyer et al. (2015).Wesuggestthatsimilarmo-
lecular studies be performed on plants that grow along nu-
trient gradients, so as to understand better the C for P
tradeoffs in different fungi and in different host plants.
Furthermore, it is now possible to use genetically modified
plants that allow different amounts of carbon transfer to the
fungus, enabling an understanding of the degree to which
the fungi reprogram sugar transporation in plant roots (e.g.
Manck-Gotzenberger and Requena 2016).
5 Indirect effects of other organisms
A final biotic factor that may result in growth depression as a
result of mycorrhizal colonization is through the influence of
these fungi on the insect and fungal antagonists of plants. AM
fungi generally increase the resistance of their host to attack by
insects and plant pathogens (Borowicz 2001; Koricheva et al.
2009). However, this is not always the case, especially with
sucking insects, where AMF can lead to increases in insect
performance. However, remarkably few studies have followed
the effects of AM fungi on insect population dynamics in the
field (but see Ueda et al. 2013). Barber et al. (2013) found that
pollinators exhibited taxon-specific responses, with honey-
bees, bumblebees, and Lepidoptera all responding differently
to AMF treatments. Koricheva et al. (2009) hint at different
responses amongst insect feeding guilds, which is to be ex-
pected from controlled experiments. Gange et al. (2003)dem-
onstrated that some AM fungal combinations increased para-
sitism by insects, some decreased it, while others had no ef-
fect. To date, no study has examined the effects of AMF on
insect community structure and the population dynamics of
herbivorous species. Without such knowledge, it is impossible
to say whether AMF effects on plants exhibit negative feed-
back as a result of enhanced populations of herbivores causing
growth depressions. Thus, long-term studies of mycorrhizal-
plant-insect interactions in field situations are urgently
needed.
Acknowledgments This study was supported by National Natural
Science Foundation of China (31270558) and the Research Funds for
the Introduction of Talents of Shanghai Science and Technology
Museum. We are grateful to the anonymous referees whose comments
greatly improved the manuscript.
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