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Commentary
It also is remarkable that qualitatively similar effects
are induced in plants by a variety of plant-associated rootcolonizing microbes, including plant growth-promoting
rhizobacteria, P. indica and mycorrhizal fungi, as summarized in Shoresh et al. (2010). This is, apparently, an example
of convergent evolution by very dissimilar organisms.
Presumably, the ability of these microbes to induce changes
in plants, resulting in a large number of healthy roots in
which they live, provides a competitive advantage.
Gary E. Harman
Department of Horticulture, Cornell University,
Geneva, NY 14456, USA
(tel +1 315 787 2452; email [email protected])
References
Alfano G, Lewis Ivey ML, Cakir C, Bos JIB, Miller SA, Madden LV,
Kamoun S, Hoitink HAJ. 2007. Systemic modulation of gene
expression in tomato by Trichoderma harzianum 382. Phytopathology 97:
429–437.
Bae H, Roberts DP, Lim H-S, Strem M, Park S-C, Ryu C-M, Melnick R,
Bailey BA. 2011. Endophytic Trichoderma isolates from tropical
environments delay disease and induce resistance against Phytophthora
capsici in hot pepper using multiple mechanisms. Molecular Plant–
Microbe Interactions, in press.
Harman GE. 2000. Myths and dogmas of biocontrol. Changes in
perceptions derived from research on Trichoderma harzianum T-22.
Plant Disease 84: 377–393.
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. 2004.
Trichoderma species – opportunistic, avirulent plant symbionts. Nature
Reviews. Microbiology 2: 43–56.
Harman GE, Mastouri F. 2010. Enhancing nitrogen use efficiency in wheat
using Trichoderma seed inoculants, Vol. 7. St. Paul, MN, USA:
International Society for Plant–Microbe Interactions, 1–4.
van Loon LC, Bakker PAHM, Pieterse CMJ. 1998. Systemic resistance
induced by rhizosphere bacteria. Annual Review of Phytopathology 36:
453–483.
Lorito M, Woo SL, Harman GE, Monte E. 2010. Translational research
on Trichoderma: from ‘omics to the field. Annual review of
Phytopathology 48: 395–417.
Marra R, Ambrosino P, Carbone V, Vinale F, Woo SL, Ruocco M,
Ciliento R, Lanzuise S, Ferraioli S, Soriente I et al. 2006. Study of
the three-way interaction between Trichoderma atroviride, plant and
fungal pathogens using a proteome approach. Current Genetics 50:
307–321.
Mastouri F. 2010. Use of Trichoderma spp. to improve plant performance
under abiotic stress. PhD thesis, Cornell University, Ithaca, NY, USA.
Mastouri F, Bjorkman T, Harman GE. 2010. Seed treatments with
Trichoderma harzianum alleviate biotic, abiotic and physiological stresses
in germinating seeds and seedlings. Phytopathology 100: 1213–1221.
Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends
in Plant Science 7: 405–410.
Segarra G, Casanova E, Bellido D, Odena MA, Oliveira E, Trillas I.
2007. Proteome, salicylic acid and jasmonic acid changes in cucumber
plants inoculated with Trichoderma asperellum strain T34. Proteomics 7:
3943–3952.
Shoresh M, Harman GE. 2008. The molecular basis of maize responses to
Trichoderma harzianum T22 inoculation: a proteomic approach. Plant
Physiology 147: 2147–2163.
2010 Cornell University
New Phytologist 2010 New Phytologist Trust
Forum
Shoresh M, Mastouri F, Harman GE. 2010. Induced systemic resistance
and plant responses to fungal biocontrol agents. Annual review of
Phytopathology 48: 21–43.
Vargas WA, Crutcher FK, Kenerley CM. 2010. Functional
characterization of a plant-like sucrose transporter from the beneficial
fungus Trichoderma virens. Regulation of the symbiotic association with
plants by sucrose metabolism inside the fungal cells. New Phytologist. 189:
777–789.
Vargas WA, Wippel R, Goos S, Kamper J, Sauer N. 2009. Plant-derived
sucrose is a key element in the symbiotic association between
Trichoderma virens and maize plants. Plant Physiology 151: 792–808.
Yedidia I, Benhamou N, Chet I. 1999. Induction of defense responses in
cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma
harzianum. Applied and Environmental Microbiology 65: 1061–1070.
Key words: abiotic plant stress, endophytic root colonists, improved plant
nitrogen use efficiency, reactive oxygen species, systemic plant disease
resistance, Trichoderma.
Trait divergence and the
ecosystem impacts of
invading species
Invasions by exotic species pose significant threats to biological
diversity, ecosystem functioning and human economies.
Ecologists have long been fascinated by the mechanisms
that allow an exotic species to establish in a new community
(e.g. Elton, 1958) and there has been growing interest in
connecting these mechanisms with the impacts of invasive
species on ecosystem functioning (Levine et al., 2003). In
this issue of New Phytologist, a recent experiment by Scharfy
et al. (pp. 818–828) compared abundant native and invasive species found in mesic herbaceous communities in
northern Switzerland. They found that while invading
species differed from native species in a few ways, they were
remarkably similar to the native species in these communities. This same pattern could be predicted in many other
plant communities based on a synthesis of theories regarding environmental influences on ecological strategies and
community assembly.
‘… species origin is not a good predictor of
competitive outcomes in communities …’
Plant functional traits are often used as proxies to determine whether species have different ecological strategies for
reproduction and resource capture (Lavorel & Garnier,
New Phytologist (2011) 189: 649–652
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Commentary
2002), and may provide mechanisms to explain which species are likely to invade, and which communities are likely
to be invaded. Several theories predict that traits of invading
species should be similar to traits of species in the native
community. Plants growing in the same area are likely to
share traits that are adaptive for the local climate because
they have experienced similar environmental selection pressures (i.e. habitat filtering; Weiher & Keddy, 1999). For
example, species growing in infertile soils tend to have slow
growth rates and increase their nutrient-use efficiency
(NUE) by having thick, well-protected leaves with long leaflongevity. Successful invaders in low-resource habitats are
likely to also have these traits (Funk & Vitousek, 2007).
Neutral theory presents the null expectation that there
should be few functional differences between native and
invading species as long as there are similar suites of traits
present in the pool of potential invaders (Daleo et al.,
2009). By contrast, there are a variety of mechanisms that
could lead to trait differences between native and invading
species. The species pool of potential invaders is likely to be
biased towards traits associated with long-distance dispersal
or desirable qualities for humans, such as good forage quality. This hypothesis is supported by trait differences between
native and invasive species found in analyses of regional and
global species pools (Leishman et al., 2007; Ordonez et al.,
2010; Van Kleunen et al., 2010). Similarly, niche-based
community assembly theory predicts that successful invasive
species should have different traits from native species; the
concept of limiting similarity assumes that exotic species
should use resources at different times or in different ways,
otherwise they would be competitively excluded from the
community (Abrams, 1983). Experiments with assembled
communities have sometimes found that functionally
distinct exotic species are more likely to successfully invade
(Fargione et al., 2003; Hooper & Dukes, 2010; but see
Emery, 2007). In addition to filling a vacant ecological
niche, invading species may be able to establish because they
are more plastic in response to resource pulses than are
native species (Davis et al., 2000; Richards et al., 2006). In
summary, these disparate theories produce a fundamental
dichotomy in predictions regarding whether traits of
invasive species should converge with species in the native
community as a result of habitat filtering or neutral processes, or diverge as a result of limiting similarity, higher
plasticity or biases in the introduced species pool (Grime,
2006).
Identifying patterns of trait divergence or convergence
may also help to predict the potential impacts of invasion;
Scharfy et al. hypothesized that invasive species would differ
from native species in a suite of traits related to ecosystem
impacts. To test this hypothesis they identified six common
invasive forb species – three annuals and three perennials –
and compared their traits with those of 12 dominant species
from the native community – six perennial forbs and six
New Phytologist (2011) 189: 649–652
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perennial graminoids. Thus, there was an inherent starting
bias in the study, in that there were so few invasive graminoids in these systems. They then screened these 18 species
for 31 traits, including commonly measured leaf-level traits,
whole-plant traits associated with resource uptake, plasticity
in response to nutrient uptake and competition, traits
related to soil impacts and allelopathic effect. To accomplish this trait screening they grew the focal species in a
series of pot experiments, and measured a subset of traits in
the field. Scharfy et al. found that the invasive forbs species
tended to be very similar to the native forbs, differing only
in having lower chlorophyll content. However, the forbs
and the graminoids varied in a number of traits, such that
the invasive forbs differed from the native graminoids by
having a suite of traits such as shorter-lived leaves with
lower tissue density and a lower NUE. As a consequence,
the foliar tissues of the invasive forbs tended to decompose
more quickly than those of the native graminoids, although
not as fast as those of the native forbs. These trait differences led the authors to conclude that invasive forbs will
alter ecosystem functioning if they invade areas dominated
by native graminoids, but will not alter ecosystem functioning in areas dominated by native forbs, as a result of the
trait similarity among forbs overall.
The comparative responses of the native vs invasive species
to nutrient fertilization and competition were among the
most surprising results in the study. A meta-analysis of
native–invasive comparisons concluded that environmental
context plays an important role in determining the relative
performance of native and invasive species, and that native
species frequently out-perform invasives when resources are
limiting (Daehler, 2003). It has nearly become dogma that
invasive species benefit more from resource enrichment than
native species, but Scharfy et al. did not find this to be the
case. Plasticity was measured in response to nutrient fertilization or competition with Holcus lanatus, a common and
strongly competitive native grass in areas of northern Europe
and a problematic invasive species in North America and
Australia. They found that the focal native and invasive
species showed similar increases in growth with fertilization,
and although the full suite of native and invasive species were
not grown in competition with one another, the invasive
species tended to have a greater growth decline when grown
in competition with a dominant grass than did the native
species. Thus, the results of this study did not support the
paradigm that successful invaders are better at pre-empting
resource pulses, contributing to a higher competitive ability.
Rather, these results suggest that species origin is not a good
predictor of competitive outcomes in communities, and
native species may frequently benefit from resource pulses if
they have traits associated with high rates of growth and
resource uptake (Maron & Marler, 2007).
Allelopathy is another mechanism that has been hypothesized to contribute to invasion. Scharfy et al. used Dactylils
2010 The Author
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Phytologist
Conclusions and future directions
Past efforts to identify trait differences between native and
invasive species did not necessarily focus on ecosystem-level
impacts; for instance, possession of small seeds may increase
the likelihood of long-distance dispersal but does not
have any a priori predicted effect on nutrient cycling rates
(Lavorel & Garnier, 2002). Each species can be characterized by a large number of functional traits. Functional traits
are frequently correlated with one another, such that suites
of traits can be used to represent ecological strategies. For
this reason, studies frequently employ multivariate clustering techniques to group species according to similar suites of
traits, or collapse the multivariate trait data onto fewer axes
that represent suites of correlated traits (e.g. Diaz et al.,
2004). These multivariate techniques can identify trait-axes
that represent the greatest trait convergence among species
(traits associated with habit filtering), and trait-axes that
identify where traits of native and invasive species diverge
(traits related to potential ecosystem impacts). If the findings
of Scharfy et al. hold in naturally assembled communities
and other ecosystem types, we might expect to find one
multivariate axis associated with habitat filtering where
invading and native species within a community are similar,
and an orthogonal axis representing potential differences
2010 Cornell University
New Phytologist 2010 New Phytologist Trust
A
Multivariate trait axis 2
(divergence = ecosystem
impacts)
glomerata as a phytometer to assess the allelopathic effects of
the focal species, by growing D. glomerata in soil in which
each focal species had been grown alone. The allelopathic
effect was calculated as the percentage decrease in D.
glomerata growth in the pre-grown soil to which activated
charcoal had or had not been added, and plants had been
fertilized. They found that invasive forbs had higher allelopathic effects than native forbs, but were similar to native
graminoids. Thus, the pattern for allelopathic effects was at
odds with the other trait differences, which tended to be
greatest between forbs and graminoids, with few differences
between the native and invasive forbs. From a niche-based
perspective, this functional difference provides an axis of
differentiation by which invasive forbs could gain a foothold when invading systems dominated by native forbs that
are functionally similar in many regards. These results
should be interpreted with some caution, however, because
the allelopathic effects were discerned through the use of
activated charcoal. Activated carbon is extremely porous
and can bind an array of complex compounds, removing
them from the soil solution. Recent work has shown that
the addition of activated carbon can stimulate microbial
activity and increase soil phosphate availability (Weißhuhn
& Prati, 2009), suggesting that the positive effects of the
addition of activated carbon may not be related to the attenuation of allelopathic effects, but rather could reflect
functional differences in the way that these species interact
with the soil microbial community.
Commentary
Forum
B
Multivariate trait axis 1
(convergence = habitat
filtering)
Fig. 1 Hypothetical multivariate trait distributions for two
communities (A, squares; B, circles) containing both native (closed
symbols) and invasive (open symbols) species, arrayed on two
primary axes. The first axis represents traits associated with similarity
among species and hence can be used to identify traits associated
with habitat filtering. Within both communities, traits of native and
invading species occupy a narrow, overlapping range, but
communities differ from one another. The second axis represents
traits associated with the greatest differences among species and can
be used to identify potential ecosystem-level impacts of invasion.
When invading and native species display trait convergence (A),
there are likely to be few ecosystem-level impacts. When invading
species have traits that diverge from native species (B), there is a
greater potential for ecosystem properties to be altered, particularly
if the invasive species reach high levels of abundance.
among native and exotic species that predict ecosystem-level
impacts (Fig. 1).
As global changes, such as invasion and climate change,
increasingly impact natural systems, a ‘Holy Grail’ of plant
ecology has become to predict how communities are likely
to respond, and feed back, to influence ecosystem-level
processes (Lavorel & Garnier, 2002; Suding et al., 2008).
We may be able to predict ecosystem-level impacts of invasion if invading species differ from native species in traits
that influence ecosystem properties, such as biogeochemical
cycling, disturbance regime, energy balance or palatability
to herbivores. Moving forward, we need a better understanding of whether the traits relating to establishment are
correlated with increased abundance of invading species.
Ultimately, invading species that become abundant and
displace native species have the greatest potential to impact
ecosystem function.
Acknowledgements
The manuscript benefited from conversations with
Elizabeth Wolkovich, for which E.E.C. was grateful.
Elsa E. Cleland
University of California, San Diego – Biology, 9500
Gilman Dr. #0116, San Diego, CA 92093, USA
(tel +1 8582460506; email [email protected])
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References
Abrams P. 1983. The theory of limiting similarity. Annual Review of
Ecology and Systematics 14: 359–376.
Daehler CC. 2003. Performance comparisons of co-occurring native and
alien invasive plants: implications for conservation and restoration.
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Daleo P, Alberti J, Iribarne O. 2009. Biological invasions and the neutral
theory. Diversity and Distributions 15: 547–553.
Davis M, Grime J, Thompson K. 2000. Fluctuating resources in plant
communities: a general theory of invasibility. Journal of Ecology 88:
528–534.
Diaz S, Hodgson JG, Thompson K, Cabido M, Cornelissen JHC, Jalili
A, Montserrat-Marti G, Grime JP, Zarrinkamar F, Asri Y et al. 2004.
The plant traits that drive ecosystems: evidence from three continents.
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Elton CS. 1958. The ecology of invasions by animals and plants. London,
UK: Methuen & Co Ltd.
Emery SM. 2007. Limiting similarity between invaders and dominant
species in herbaceous plant communities? Journal of Ecology 95: 1027–1035.
Fargione J, Brown C, Tilman D. 2003. Community assembly and
invasion: an experimental test of neutral versus niche processes.
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Funk JL, Vitousek PM. 2007. Resource-use efficiency and plant invasion
in low-resource systems. Nature 446: 1079–1081.
Grime JP. 2006. Trait convergence and trait divergence in herbaceous
plant communities: mechanisms and consequences. Journal of Vegetation
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Hooper DU, Dukes JS. 2010. Functional composition controls invasion
success in a California serpentine grassland. Journal of Ecology 98: 764–777.
Lavorel S, Garnier E. 2002. Predicting changes in community
composition and ecosystem functioning from plant traits: revisiting the
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New
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Leishman MR, Haslehurst T, Ares A, Baruch Z. 2007. Leaf trait
relationships of native and invasive plants: community- and global-scale
comparisons. New Phytologist 176: 635–643.
Levine J, Vila M, D’Antonio C, Dukes J, Grigulis K, Lavorel S. 2003.
Mechanisms underlying the impacts of exotic plant invasions. Proceedings
of the Royal Society of London Series B-Biological Sciences 270: 775–781.
Maron J, Marler M. 2007. Native plant diversity resists invasion at both
low and high resource levels. Ecology 88: 2651–2661.
Ordonez A, Wright IJ, Olff H. 2010. Functional differences between
native and alien species: a global-scale comparison. Functional Ecology
24: 1353–1361.
Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M. 2006.
Jack of all trades, master of some? On the role of phenotypic plasticity in
plant invasions. Ecology Letters 9: 981–993.
Scharfy D, Funk A, Olde Venterink H, Güsewell S. 2011. Invasive forbs
differ functionally from native graminoids, but are similar to native
forbs. New Phytologist 189: 818–828.
Suding KN, Lavorel S, Chapin FS, Cornelissen JHC, Dı́az S, Garnier E,
Goldberg D, Hooper DU, Jackson ST, Navas M-L. 2008. Scaling
environmental change through the community-level: a trait-based
response-and-effect framework for plants. Global Change Biology 14:
1125–1140.
Van Kleunen M, Weber E, Fischer M. 2010. A meta-analysis of trait
differences between invasive and non-invasive plant species. Ecology
Letters 13: 235–245.
Weiher E, Keddy P, eds. 1999. Ecological assembly rules: perspectives,
advances, retreats. New York, NY, USA: Cambridge University Press.
Weißhuhn K, Prati D. 2009. Activated carbon may have undesired side
effects for testing allelopathy in invasive plants. Basic and Applied Ecology
10: 500–507.
Key words: community assembly, convergence, divergence, ecosystem
impact, functional traits, habitat filtering, invasion.
Letters
Effect of segregation and
genetic exchange on
arbuscular mycorrhizal fungi
in colonization of roots
Introduction
Arbuscular mycorrhizal fungi (AMF) are abundant soil
organisms and form symbioses with roots of the majority of
terrestrial plants (Smith & Read, 2008). The symbiosis with
AMF can promote plant productivity and diversity, and
tolerance to pathogens and to herbivores (Newsham et al.,
1995; van der Heijden et al., 1998; Bennett et al., 2006;
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Bennett & Bever, 2007). The hyphae produced by spores
are coenocytic, harbouring many nuclei in a common cytoplasm. Moreover, genetic differences among co-occurring
nuclei have been observed and this explains the high intraindividual genetic diversity found in AMF (Pringle et al.,
2000; Clapp et al., 2001; Kuhn et al., 2001; Rodriguez
et al., 2004; Hijri & Sanders, 2005). Two processes related
to the within-individual genetic variation in AMF have
been recently demonstrated in the species Glomus
intraradices and can affect the nucleotype content of an
AMF in a very short time span (Croll et al., 2009; Angelard
et al., 2010). First, genetic exchange between two genetically different AMF lines can lead to new spores having a
mixture of parental nucleotypes (Croll et al., 2009).
Second, one mother spore can produce new spores with
different nucleotype contents as a result of the segregation
of nucleotypes at spore formation (Angelard et al., 2010).
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