ΠΡΟΓΡΑΜΜΑ ΔΙΑ ΒΙΟΥ ΜΑΘΗΣΗΣ ΑΕΙ ΓΙΑ ΤΗΝ
ΕΠΙΚΑΙΡΟΠΟΙΗΣΗ ΓΝΩΣΕΩΝ ΑΠΟΦΟΙΤΩΝ ΑΕΙ
(ΠΕΓΑ)
«Οι σύγχρονες τεχνικές βιο-ανάλυσης στην υγεία, τη
γεωργία, το περιβάλλον και τη διατροφή»
PP62CH10-Smith1 ARI 4 April 2011 14:56
Roles of Arbuscular
Mycorrhizas in Plant
Nutrition and Growth:
New Paradigms from Cellular
to Ecosystem Scales
Sally E. Smith and F. Andrew Smith
Soils Group, School of Agriculture, Food and Wine, University of Adelaide, Waite Campus,
Adelaide, South Australia 5005, Australia; email: sally.smith@adelaide.edu.au,
andrew.smith@adelaide.edu.au
Annu. Rev. Plant Biol. 2011. 62:227–50
First published online as a Review in Advance on
March 7, 2011
The Annual Review of Plant Biology is online at
plant.annualreviews.org
This article’s doi:
10.1146/annurev-arplant-042110-103846
Copyright
c
2011 by Annual Reviews.
All rights reserved
1543-5008/11/0602-0227$20.00
Keywords
plant nutrient uptake pathways, phosphorus uptake, nitrogen uptake,
mycorrhizal growth responses
Abstract
Root systems of most land plants form arbuscular mycorrhizal (AM)
symbioses in the field, and these contribute to nutrient uptake. AM
roots have two pathways for nutrient absorption, directly through the
root epidermis and root hairs and via AM fungal hyphae into root corti-
cal cells, where arbuscules or hyphal coils provide symbiotic interfaces.
New physiological and molecular evidence shows that for phospho-
rus the mycorrhizal pathway (MP) is operational regardless of plant
growth responses (positive or negative). Amounts delivered cannot be
determined from plant nutrient contents because when responses are
negative the contribution of the direct pathway (DP) is reduced. Nitro-
gen (N) is also delivered to roots via an MP, but the contribution to total
N requirement and the costs to the plant are not clear. The functional
interplay between activities of the DP and MP has important implica-
tions for consideration of AM symbioses in ecological, agronomic, and
evolutionary contexts.
227
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Further
ANNUAL
REVIEWS
PP62CH10-Smith1 ARI 4 April 2011 14:56
Glomeromycota: the
phylum of fungi to
which the arbuscular
mycorrhizal fungi
belong
Contents
INTRODUCTION.................. 228
STRUCTURAL DIVERSITY IN
ARBUSCULAR MYCORRHIZAL
SYMBIOSES: FUNCTIONAL
IMPLICATIONS................. 229
Intraradical Colonization . . . . . . . . . . . 229
Development of Arbuscular
Mycorrhizal Fungal Mycelium
inSoil.......................... 230
Root and Fungus Provide Two
Pathways for Nutrient Uptake . . . 230
FUNCTIONAL DIVERSITY
OF AM SYMBIOSES. . . . . . . . . . . . . . 231
FOCUS ON PHOSPHORUS
NUTRITION..................... 233
Forms and Availability of
Phosphorus in Soil . . . . . . . . . . . . . . 233
Uptake and Translocation of
Phosphate by Arbuscular
Mycorrhizal Fungal Hyphae and
Delivery to Intraradical
Interfaces. . . . . . . . . . . . . . . . . . . . . . . 233
Hidden Phosphate Uptake:
Contributions of Mycorrhizal and
Direct Pathways for Uptake . . . . . 235
Changes in Orthophosphate
Transporter Gene Expression in
Arbuscular Mycorrhizal Roots . . . 236
ARBUSCULAR MYCORRHIZAL
SYMBIOSES AND NITROGEN
NUTRITION..................... 237
InorganicNitrogen................ 237
OrganicNitrogen.................. 239
IMPLICATIONS OF NEW
PARADIGMS AT WHOLE
PLANTLEVEL.................. 240
TOWARD MORE REALISTIC
SCALINGUP?................... 241
INTRODUCTION
Arbuscular mycorrhizas, which involve ap-
proximately 80% of terrestrial plant species
and obligately symbiotic fungi in the phylum
Glomeromycota, are the most common and
widespread terrestrial plant symbioses. They
are extremely ancient (>450 million years), rep-
resenting a very long period of coevolution and
indicating considerable selective advantage of
the symbiosis for both partners (134). Arbuscu-
lar mycorrhizal (AM) symbioses are biotrophic
and also (usually) mutualistic, based on bidi-
rectional transfers of organic carbon (C) from
the plant and soil-derived nutrients [particu-
larly phosphorus (P) but also nitrogen (N) and
zinc (Zn) from the fungi] (76, 134).
With the exception of plants that form other
types of mycorrhiza (ecto-, ericoid, and orchid
mycorrhiza) and the relatively few species that
are never mycorrhizal (151), the AM condition
is normal for plants growing in most field sit-
uations. The nonmycorrhizal (NM) condition
is found naturally only under extreme soil con-
ditions (e.g., highly disturbed or waterlogged
soils) and is therefore not usually the control sit-
uation but rather the treatment (as with plants
grown experimentally in sterilized soil). Recog-
nition that the NM state is very unusual in na-
ture should alter perspectives of the r oles of
AM in plant function and their evolutionary
persistence.
The last review in this series specifically ad-
dressing physiology of AM symbioses was pub-
lished over 20 years ago (132). Since then cellu-
lar and molecular research has led to enormous
advances in knowledge of signaling and cellular
interactions between the symbionts, control
of development of AM symbioses, and the
expression and function of genes involved (10,
12, 50, 106, 107). Ecologists have increasingly
become aware of t he likely significance of AM
symbioses in nature but have (mainly) tended
to ignore underground symbiosis-driven pro-
cesses, even though effective prediction of plant
responses to changed conditions (e.g., competi-
tion) requires an understanding of mechanisms
(74). Together with agronomists, they have
often relied on well-entrenched functional
models to interpret potential roles of arbuscular
mycorrhizas in plant interactions and produc-
tivity. Physiological experiments over the past
10–15 years, coupled with molecular biology
228 Smith
·
Smith
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PP62CH10-Smith1 ARI 4 April 2011 14:56
Symbiosis: the living
together of two
dissimilar organisms;
includes a spectrum of
interactions from
beneficial to
detrimental
Biotrophic:
a symbiotic organism
that obtains nutrients
from the living cells of
its partner
Mutualistic:
a symbiosis that is
beneficial to both
partners
Mycorrhiza: literally
“fungus-root,” a
symbiosis between
specialized soil fungi
and roots or other
underground organs of
land plants
Mycelium: network
of branching hyphae
Arbuscule: ahighly
branched structure
formed inside root
cells by arbuscular
mycorrhizal fungi;
creates a large
interface between
fungus and plant
Hyphae: long,
branching, tubular
structures formed by
fungi
and advanced microscopy, have provided new
information that has overturned many aspects
of these established models. This new infor-
mation includes the range of fungal structures
formed between AM fungi and plant roots (22);
the diversity of growth responses to AM colo-
nization, from highly positive to negative (75,
76); and the significance and contribution of
the mycorrhizal uptake pathway in delivering
nutrients (particularly P) to plants, regardless
of whether they respond positively or not (126).
We now bring together this new research to
provide a better picture of the integration of
plant and AM fungal nutritional processes that
contribute to plant growth and productivity.
The outcomes have important implications for
understanding AM symbiosis at scales from
cellular through whole plant to ecological
interactions.
STRUCTURAL DIVERSITY IN
ARBUSCULAR MYCORRHIZAL
SYMBIOSES: FUNCTIONAL
IMPLICATIONS
Intraradical Colonization
An AM fungus lives in two environments, the
root from which it receives organic C and to
which it delivers nutrients, and the soil from
which it absorbs those nutrients. The intrarad-
ical mycelium (IRM) grows in an environment
controlled by plant homeostasis, whereas the
extraradical mycelium (ERM) encounters con-
siderable environmental variations, such as soil
pH, nutrient availability, and soil moisture.
Colonization of roots by AM fungi in-
volves subtle signaling between the symbionts,
leading to expression of key genes and tightly
programmed cellular events (10, 50, 106, 107).
The outcome is considerable fungal growth in
the root cortex, where interfaces involved in
nutrient exchange develop. A varied range of
structures is formed by AM fungi in the roots of
plants, as first highlighted by Gallaud (32). Use
of a relatively small number of species of plants
and AM fungi led to the belief that arbuscules,
which are terminal, dichotomously branched,
cab
A
IH
CS
R
Figure 1
Photomicrographs of arbuscular mycorrhizal colonization of tomato roots (a,b)
and extraradical mycelium (c). (a) Intercellular hyphae (IH) of Glomus
intraradices leading to arbuscules (A) in cortical cells; (b) intracellular hyphal
coils (C) of Gigaspora rosea;(c) extraradical mycelium of an AM fungus (arrow)
growing between a root (R) and a soil particle (S). Panels (a,b)arefromSmith
et al. (138), reproduced with permission of New Phytologist. Panel (c)isfrom
Olsson et al. (103), reproduced with permission of Springer-Verlag.
intracellular fungal structures (Figure 1a),
are the sole defining feature of an arbuscular
mycorrhiza. Dependence on arbuscules for
definitive identification of an AM root and
failure to recognize the common occurrence
and importance of intracellular coiled hyphae
(Figure 1b) as alternative AM structures has
almost certainly led to underestimation of the
number of plant species that form arbuscular
mycorrhizas in nature (128). Demonstration
that hyphal coils, arbuscules, and intermediate
structures are involved in the nutrient transfers
that underpin a functional symbiosis has been
a major step forward (16, 21, 22, 33, 78, 128).
Experiments show that identities (and hence
genomes) of both plant and fungal partners
determine the mycorrhizal type (14, 21, 22).
Intracellular fungal growth involves devel-
opment of specialized cytoplasmic assemblies
that ultimately lead to formation of symbiotic
interfaces, including marked invagination, in-
crease in surface area of contact, and modifica-
tion of the plant plasma membrane to form a
perifungal membrane [or periarbuscular mem-
brane (PAM) when associated with arbuscules]
(33, 34). The fungus remains outside the plant
cytoplasm such that the symbiotic interfaces in-
volve plasma membranes of both fungus and
plant, separated by an apoplastic compartment
(Figure 2) that has an acidic pH and contains
some modified plant wall material (7, 136). The
plant membranes are strongly modified, par-
ticularly in association with arbuscule forma-
tion. Variations in location of specialized mem-
brane domains surrounding AM structures of
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•
Arbuscular Mycorrhizas in Plant Nutrition and Growth 229
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PP62CH10-Smith1 ARI 4 April 2011 14:56
P depletion
Direct
pathway
Mycorrhizal pathway
H
+
PiPi Pi
Symbiotic interface
Apoplast
Extraradical
mycelium
Plant cell
AMF
Colonized
cortical cell
Pi transporters
H
+
-ATPase
High-anity
Pi transporters
AM fungal
High-anity
Pi transporters
Unknown
mechanism
KEY
Figure 2
Diagrammatic representation of the direct and mycorrhizal orthophosphate
(Pi) uptake pathways in an arbuscular mycorrhizal (AM) root. The direct
pathway (DP) involves high-affinity Pi transporters located in root hairs and
epidermal cells near the root apex. DP activity results in progressive depletion
of Pi concentration close to roots (dashed black line) because uptake is faster than
replacement by diffusion or mass flow. The mycorrhizal pathway (MP) develops
behind the root hair zone. It involves uptake of Pi by AM fungal high-affinity
Pi transporters in the extraradical mycelium (ERM), followed by translocation
of phosphorus (P) along the hyphae to intracellular structures in the root cortex
and transfer to the root. Inset shows transfer across the symbiotic interface,
which involves efflux of Pi from the arbuscular mycorrhizal fungus (or AMF, by
unknown mechanism; black square) into the apoplast and uptake into the plant
cells by Pi transporter(s) that are preferentially or specifically expressed in
colonized cortical cells. H
+
-ATPases are involved at all Pi-uptake steps (shown
only in the symbiotic interface). Activity of the MP results in extension of the
phosphate depletion zone as far as the ERM extends. The MP may also operate
in nitrogen (N) uptake (see also Figure 4). Based on a diagram b y E.J. Grace.
different types (arbuscules, coils, and intercel-
lular hyphae when present) probably occur (78,
110). The consequences of variation remain to
be fully explored, but a key conclusion is that
arbuscules are not the only AM fungal struc-
tures having significant functional interfaces
with plant cortical cells. Physiological, molecu-
lar, and field studies must include awareness of
this diversity to gain a better picture of the oc-
currence and function of different types of AM
colonization of wild and cultivated plants.
Development of Arbuscular
Mycorrhizal Fungal Mycelium in Soil
The ERM (Figure 1c) plays critical roles in up-
take and rapid translocation of nutrients to the
intraradical structures and in foraging to locate
new roots on the same or different plants, which
are new sources of organic C (103). Mycelia
produced by different fungi have quite varied
characteristics, in terms of hyphal diameters
(usually in the range of 2–20 μm), extent of
growth away from the root, and ability to ab-
sorb nutrients at a distance [up to 25 cm (65)]
and translocate them to the root (23, 63, 99,
127). Many AM fungi produce runner hyphae
of relatively large diameter that can subtend
tufts of finely branched hyphae; the latter turn
over rapidly and are probably involved in nutri-
ent uptake (4). Hyphal length densities in soil
associated with plants in pot experiments are
variable and usually in the range of 1–40 m g
−1
depending at least in part on the identity of the
AM fungus (61, 99, 138). They are very much
higher than the root length densities of asso-
ciated plants [e.g., 2.6 versus 0.04 m g
−1
for
AM fungal hyphae and wheat roots, respectively
(89)], emphasizing how effectively the fungi can
explore soil. Implications of variability in struc-
ture and function of the ERM are becoming
recognized, and it appears that where several
fungi colonize a root (as is normal in the field),
their nutrient acquisition activities are comple-
mentary (66, 81).
The ERM may be associated with several
plants of the same or different species, forming
an interconnected network (62, 134). Hyphae
from the same fungal mycelium, and sometimes
from different isolates of the same species, can
anastomose (fuse) frequently. This process al-
lows for exchange of nuclei, network repair, and
fusion of two or more separate mycelia into
larger units facilitating transfer of phosphorus
(P) (2, 62, 97). The extent of sharing of costs and
benefits of a common mycelial network among
the symbionts requires further research.
Root and Fungus Provide Two
Pathways for Nutrient Uptake
An AM root superficially retains many of the
structural features of an NM root. Root apex,
epidermis, root hairs, and lateral root branches
remain recognizable. Root hairs still occur on
AM roots, although their length and density
may be lower than in equivalent NM plants
230 Smith
·
Smith
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