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these species and there are active breeding programmes
around the world for these traits. Peach is particularly
amenable for forward genetic studies because it has a small
genome (approximately half the size of the P. trichocarpa
genome) with little duplication history, is self-fertile, has a
generation time as short as 2–4 yr and significant genomic
resources are available (Shulaev et al., 2008). Recent work
has demonstrated the utility of peach to map and sequence
candidate genes for important winter-dormancy traits
(Bielenberg et al., 2008; Fan et al., 2010). Apple, in turn,
possesses a very robust transformation capability for reverse
genetics (Shulaev et al., 2008).
Research on several species will be needed to truly understand ecosystem-level phenological responses to climate
change because induction of growth cessation, bud set and
bud flush is regulated differently in different species. For
example, in Malus and Pyrus spp. growth cessation and bud
set appear to be regulated by low temperatures alone without
the involvement of photoperiod (Heide & Prestrud, 2005).
While trees dominate the discussion of perenniality, many
herbaceous species also develop buds and enter winter
dormancy, often from underground structures (Horvath
et al., 2002). It is clear that parallel work on multiple plant
systems will be important to incorporate the biological
diversity of perennial species. The community of perennial
biology researchers will need to continue to be adept at applying data and concepts gained from one system to another.
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Horvath DP, Chao WS, Anderson JV. 2002. Molecular analysis of signals
controlling dormancy and growth in underground adventitious buds of
leafy spurge. Plant Physiology 128: 1439–1446.
Lubbock J. 1899. On buds and stipules. London, UK: Kegan Paul, Trench,
Trubner & Co. Ltd.
Olsen JE. 2003. Molecular and physiological mechanisms of bud dormancy
regulation. In: Tanino KK, ed. XXVI international horticultural congress –
environmental stress. Toronto, Canada: ISHS, 437–453.
Rohde A, Storme V, Jorge V, Gaudet M, Vitacolonna N, Fabbrini F,
Ruttink T, Zaina G, Marron N, Dillen S et al. 2010. Bud set in poplar
– genetic dissection of a complex trait in natural and hybrid populations.
New Phytologist 189: 106–121.
Shulaev V, Korban SS, Sosinski B, Abbott AG, Aldwinckle HS, Folta
KM, Iezzoni A, Main D, Arus P, Dandekar AM et al. 2008. Multiple
models for Rosaceae genomics. Plant Physiology 147: 985–1003.
Tanino KK, Kalcsits L, Silim S, Kendall E, Gray GR. 2010. Temperaturedriven plasticity in growth cessation and dormancy development in
deciduous woody plants: a working hypothesis suggesting how molecular
and cellular function is affected by temperature during dormancy
induction. Plant Molecular Biology 73: 49–65.
Taylor G. 2002. Populus: Arabidopsis for forestry. Do we need a model
tree? Annals of Botany 90: 681–689.
Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U,
Putnam N, Ralph S, Rombauts S, Salamov A et al. 2006. The genome
of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:
1596–1604.
Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D,
Pindo M, FitzGerald LM, Vezzulli S, Reid J et al. 2007. A high quality
draft consensus sequence of the genome of a heterozygous grapevine
variety. PLoS ONE 2(12): e1326. doi:10.1371/journal.pone.0001326.
Key words: bud, genome, perennial, photoperiod, seasonal, transcriptome,
tree.
Douglas G. Bielenberg
Clemson University – Horticulture, 152 Poole Agricultural
Center, Clemson, SC 29631-0319, USA
(tel +1 864 656 4968; email [email protected])
References
Battey NH. 2000. Aspects of seasonality. Journal of Experimental Botany
51: 1769–1780.
Bielenberg DG, Wang Y, Li Z, Zhebentyayeva T, Fan S, Reighard GL,
Scorza R, Abbott AG. 2008. Sequencing and annotation of the
evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a
cluster of six MADS-box transcription factors as candidate genes for
regulation of terminal bud formation. Tree Genetics and Genomes 4:
495–507.
Fan S, Bielenberg DG, Zhebentyayeva TN, Reighard GL, Okie WR,
Holland D, Abbott AG. 2010. Mapping quantitative trait loci
associated with chilling requirement, heat requirement and bloom date
in peach (Prunus persica). New Phytologist 185: 917–930.
Heide OM, Prestrud AK. 2005. Low temperature, but not photoperiod,
controls growth cessation and dormancy induction and release in apple
and pear. Tree Physiology 25: 109–114.
Horvath D. 2009. Common mechanisms regulate flowering and
dormancy. Plant Science 177: 523–531.
Horvath DP, Anderson JV, Jia Y, Chao WS. 2005. Cloning,
characterization, and expression of growth regulator CYCLIN
D3-2 in leafy spurge (Euphorbia esula). Weed Science 53:
431–437.
2011 The Authors
New Phytologist 2011 New Phytologist Trust
Solving the conundrum of
plant species coexistence:
water in space and time
matters most
Ecologists still wonder how so many competing plant
species can coexist at the same site, defying the competitiveexclusion principle. All plants use and compete for the same
basic resources (light, CO2, water, nutrients and space for
growth); species with competitive advantage reduce resource
availability for other species that will experience difficulties
becoming established or remaining. However, if species
sufficiently partition the abiotic and biotic environments, or
if there are trade-offs in resource allocation (e.g. some species
may allocate more resources to increase reproduction,
whereas others might allocate more resources to survival or
to growth), then different species can coexist by using
different ranges and proportions of resources (Pacala &
Tilman, 1994). The classical answer of this species coexistence conundrum states that stable coexistence between
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competing species requires them to occupy different niches.
But the niche concept, which was initially conceived by
zoologists and emphasized the role of habitat and food in
defining an animal’s niche (Chase & Leibold, 2002), does
not offer an obvious explanation for coexistence among
plants, because all plants use, and compete for, the same
aforementioned resources and acquire them in similar ways.
The question thus remains as to how competing plant
species coexist apparently without the niche differences that
classical theory predicts to be necessary. Apart from quantitative refinements (for instance, considering the differential
resource consumption rate of species) and successional
dynamics, two answers are possible: either the classical
theory is wrong or incomplete and stabilizing mechanisms
are unimportant (neutral models; Hubbell, 2001; de Aguiar
et al., 2009), or there are niche differences between plants
that have been overlooked (Silvertown, 2004). Plant ecologists keep trying to solve this question, most of them
looking for the separation of niches and the quantification
of the extent of the differences between two niches in order
for corresponding species to coexist (Begon et al., 2006). In
this issue of New Phytologist, Araya et al. (pp. 253–258)
have elegantly shown separation of hydrological niches in
two very different plant communities (in British wet meadows
and in South African fynbos), quantified them and interestingly suggested the ecohydrological axis as potentially one of
the most general drivers of niche differentiation for plants.
‘... the underlying mechanisms are ecophysiologically
fundamental to plants and have the potential to
govern niche segregation in many other communities.’
The ‘habitat’ niche of a plant species may be defined as a
spatial and temporal function of the ranges of water, light,
nutrient, temperature and competition with neighbours
that the plant is able to live with. This definition is made
within large gradients of availability for each resource –
arid–humid (water), oligotrophic–eutrophic (nutrients),
shade–sun (light) and cold–hot (temperature) – and also as
a function of microsite heterogeneity, climatic variability
and disturbance that further contribute to generate local
diversity. However, altogether the mechanisms that stabilize
communities through such niche segregation merit further
explanation (Chesson, 2000; Adler et al., 2007). Many such
mechanisms have been proposed, and more than one may
function simultaneously in particular plant communities. A
few years ago, Silvertown et al. (1999) showed that segregation on hydrological gradients occurs in European wet
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meadows and that specialization of species into distinct
niches is a result of a trade-off between tolerance of aeration
stress and tolerance of drying stress. Araya et al. have now
expanded this seminal work, testing this mechanism by
quantifying the hydrological niches of floristically, functionally and phylogenetically distinct plants in fynbos
communities in the Cape of South Africa. They have found
this coinciding trade-off, supporting the existence of the
same physiological constraints, and strengthening the generality of hydrological niche segregation.
As pointed out by Araya et al., hydrological niche segregation occurs in a great variety of vegetation types across the
entire spectrum of environments, from wet or mesic to arid.
Araya et al.’s work connects such a single trade-off between
aeration and water stress from a community (wet meadows),
where aeration stress would be the limiting factor, to an
ecologically and geographically distant one (South-African
fynbos) where water stress is the rule. This result strongly
suggests that the underlying mechanisms are ecophysiologically fundamental to plants and have the potential to
govern niche segregation in many other communities. One
probable mechanism is the competing demand of water conservation vs carbon acquisition along soil moisture gradients.
Another mechanism is the need of nutrient acquisition along
nutrient gradients that are correlated with soil moisture gradients. The first mechanism is a consequence of the fact that
plants must regulate water loss through stomata while they
acquire the CO2 required for photosynthesis and growth.
Water use efficiency (WUE), the ratio of CO2 assimilated : stomatal conductance, should thus vary between
species in a systematic manner along soil moisture gradients.
Nutrient availability changes along soil moisture gradients,
with a maximum in mesic soils and minima in waterlogged
and very dry conditions (Araya, 2005). Plants must allocate
resources to roots to compete successfully for nutrients, but
to shoots to compete for light, and thus a nutrient gradient
engenders a trade-off that forces plants to specialize. These
fine-scale hydrological gradients are thus strongly linked to
the ‘biogeochemical’ niche, defined as the species position in
the multivariate space generated by their content, not only of
macronutrients such as nitrogen (N), phosphorus (P) or
potassium (K), but also of micronutrients such as molybdenum (Mo), magnesium (Mg) and calcium (Ca), and trace
elements such as lead (Pb) and arsenic (As) (Peñuelas et al.,
2008). Usually, there is a strong differentiation in the total
and relative (stoichiometry) content of the different elements
in coexisting plant species, and, there is, moreover, a differential species-specific plasticity in the response of this
elemental composition to changes in environmental conditions (Peñuelas et al., 2008).
Araya et al. define the hydrological niche segregation as
partitioning of space on fine-scale soil-moisture gradients,
and as partitioning of water as a resource through different
acquisition strategies, such as different phenologies or root-
2011 The Authors
New Phytologist 2011 New Phytologist Trust
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ing depths. By using the variable ‘sum of exceedance value’
relative to the threshold depths of each site for both aeration
and water stress, they quantify the niche segregation and
capture all three components of soil moisture variation in
space, depth and time. Nevertheless, in order to capture
more comprehensively this latter temporal component of
niche partitioning, we propose that the variance in the
intensity and seasonal distribution of both these aeration
and water stress ‘exceedances’ should also be considered
because such variances may play a significant additional or
synergic niche segregation role. The ecological rationale for
enhanced coexistence with increasing variances or fluctuations (‘fluctuation’ niche; Terradas et al., 2009) is based on
the different growth response of species to water availability.
If water availability fluctuates, the temporal advantage of
one species becomes balanced by the advantage of the other
species at another time, but if water availability remains
constant, competitive exclusion is more likely to occur. A
good example of the importance of the ‘fluctuation niche’
and of the presence of different syndromes is found in the
Mediterranean environment (Fig. 1), which shows characteristic large seasonal and interannual rain fluctuations
(Terradas et al., 2009). As a result, the depth of roots profoundly affects the variance of water availability, which in
turn affects the variance of nutrient availability and the
variances in the leaf water and nutrient status (Filella &
Peñuelas, 2003). In fact, the main division in
Mediterranean communities is established between species
with deep roots, with more constant water and nutrient
resources, and species with shallow roots, which use
episodic rainwater and associated nutrient uptake. Plants
develop several responses between the two extremes of this
constant–episodic gradient. At one extreme there is a great,
but slow, development of permanent vertical structure, both
aboveground and belowground, to ensure minimum
between-year and between-season fluctuation in availability
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of resources. At the other extreme there is a high turnover
of structural components, mostly leaves and roots, as a
result of high growth rates in favourable periods, which is
associated with the existence of short life cycles and small
plants when water resources are persistently scarce or when
disturbances preclude the development of continuous canopies by larger plants. Thus, there is a gradient from a
conservative strategy, when fluctuations are scarce, to an
opportunistic strategy, which withstands larger fluctuations
with a more discontinuous activity. Thermodynamically,
conservative species use the resources more efficiently with
less energy dissipation, obtaining greater benefit at the end
of succession (Margalef, 1997). However, disturbances
allow different strategies to occur simultaneously and to
configure complementarily the communities.
There are other drivers of niche segregation linked to the
temporal axis. Species could coexist even in temporally and
spatially homogeneous environments, because the mechanisms of coexistence differ throughout the developing stages
of the species’ life history (Nakashizuka, 2001). The socalled ‘life history’ basis for niche segregation considers the
different developing stages of a species as well as the different species’ life span and size. Obviously, the interactions of
the ‘habitat’ with the ‘fluctuation’ and the ‘life history’ components geometrically increase the number of possible
niches enhancing segregation. Variation at the individual
scale further explains why large numbers of intensely competing species coexist (Clark, 2010).
In any case, as the authors comment, their results emphasize the well-known importance of soil moisture and
hydrology for structuring plant communities through space
and time, which therefore has implications for the conservation of plant communities that now face changing
hydrological conditions caused by water extraction and
climate change (IPCC, 2007). These results should thus be
considered not only in niche ecological studies trying to disentangle the conundrum of plant species coexistence, but
also in the risk assessment of climate and environmental
change impacts on species richness. Of course, the main
message of this interesting and elegant study of Araya et al.
is to remind us once more of the fundamental role of water
availability in space and time to shape life in Earth.
Josep Peñuelas1*, Jaume Terradas2 and
Francisco Lloret2
1
Fig. 1 Mediterranean shrubland in the Prades mountains (Catalonia,
north-east Spain) with many competing plant species coexisting in
the same site, thus defying the competitive-exclusion principle.
2011 The Authors
New Phytologist 2011 New Phytologist Trust
Global Ecology Unit CREAF-CEAB-CSIC, Edifici C,
Universitat Autònoma de Barcelona,
08193 Bellaterra, Spain;
2
CREAF (Center for Ecological Research and Forestry
Applications), Edifici C, Universitat Autònoma de
Barcelona, 08193 Bellaterra, Spain
(*Author for correspondence: tel +34935812199(1312);
email [email protected])
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Commentary
Acknowledgements
The research conducted by the authors is supported by the
Spanish Government projects CGL2006-04025 ⁄ BOS,
CGC2010-17172 and Consolider Ingenio Montes
(CSD2008-00040), by the European project NEU
NITROEUROPE (GOCE017841), and by the Catalan
Government project SGR 2009-458.
The nexus of host and
pathogen phenology:
understanding the disease
triangle with climate change
References
Adler PB, HilleRisLambers J, Levine JM. 2007. A niche for neutrality.
Ecology Letters 10: 95–104.
de Aguiar MAM, Baranger M, Baptestini EM, Kaufman L, Bar-Yam Y.
2009. Global patterns of speciation and diversity. Nature 460:
384–387.
Araya YN. 2005. Influence of soil-water regime on nitrogen availability and
plant competition in wet-meadows. PhD thesis, Open University, Milton
Keynes, UK.
Araya YN, Silvertown J, Gowing DJ, McConway KJ, Linder HP,
Midgley G. 2010. A fundamental, eco-hydrological basis for
niche segregation in plant communities. New Phytologist 189:
253–258.
Begon M, Colin R, Townsend R, Harper JL. 2006. Ecology. From
individuals to ecosystems. Oxford, UK: Blackwell Publishing.
Chase JM, Leibold MA. 2002. Spatial scale dictates the productivitybiodiversity relationship. Nature 416: 427–430.
Chesson P. 2000. Mechanisms of maintenance of species diversity. Annual
Review of Ecology and Systematics 31: 343–366.
Clark J. 2010. Individuals and the variation needed for high species
diversity in forest trees. Science 327: 1129–1132.
Filella I, Peñuelas J. 2003. Partitioning of water and nitrogen in
co-occurring species of a mediterranean shrubland. Oecologia 137:
51–61.
Hubbell SP. 2001. The unified neutral theory of biodiversity and
biogeography. Princeton, NJ, USA: Princeton University Press.
IPCC. 2007. Solomon S, Qin D, Manning M, Chen Z, Marquis M,
Averyt KB, Tignor M, Miller HL, eds. Climate change 2007: the physical
science basis. Contribution of Working Group 1 to the fourth assessment
report of the Intergovernmental Panel on climate change. Cambridge, UK
& New York, NY, USA: Cambridge University Press.
Margalef R. 1997. Our biosphere. D-21385 Oldendorf ⁄ Luhe, Germany:
Ecology Institute.
Nakashizuka T. 2001. Species coexistence in temperate, mixed deciduous
forests. Trends in Ecology and Evolution 16: 205–210.
Pacala SW, Tilman D. 1994. Limiting similarity in mechanistic and
spatial models of plant competition in heterogeneous environments. The
American Naturalist 143: 222–257.
Peñuelas J, Sardans J, Ogaya R, Estiarte M. 2008. Nutrient stoichiometric
relations and biogeochemical niche in coexisting plant species: effect of
simulated climate change. Polish Journal of Ecology 56: 613–622.
Silvertown J. 2004. Plant coexistence and the niche. Trends in Ecology and
Evolution 19: 605–611.
Silvertown J, Dodd ME, Gowing D, Mountford O. 1999.
Hydrologically-defined niches reveal a basis for species-richness in plant
communities. Nature 400: 61–63.
Terradas J, Peñuelas J, Lloret F. 2009. The fluctuation niche in plants.
International Journal of Ecology 2009: ID 959702, doi: 10.1155/2009/
959702.
Key words: diversity, fluctuation niche, hydrological niche, life history,
niche, nutrients, species coexistence, sum of exceedance value.
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We have observed a remarkable increase in large-scale,
sudden onset of decline (unknown causes) and known disease
(bacterial, fungal, viral) outbreaks in the last few decades,
with more predicted globally (Ganley et al., 2009). Increases
in temperature, changes in the timing and effectiveness of
precipitation, the change in the frequency and intensity of
other, catastrophic events (e.g. windthrows, tornadoes, bark
beetle outbreaks) and invasions of both native and exotic
pathogens have thrown unlikely combinations of host
plants, plant pathogens and environmental variability
together with unpredicted outcomes. A recent canker outbreak in Alnus tenuifolia in interior Alaska, associated with
the hot, dry summer of 2004 (Ruess et al., 2009), has refocused attention on the role of temperature and drought in
canker incidence (Schoeneweiss, 1975). In this issue of New
Phytologist, Rohrs-Richey et al. (pp. 295–307) open a new
line of research in host–pathogen relationships with clarity:
an experimental test of the intersection of the phenology of
host susceptibility (Alnus fruticosa), the life cycle of the pathogen (Valsa melanodiscus) and environmental variability
(temperature, drought).
‘For the first time, Rohrs-Richey et al. quantified the
reduction in transpiration directly attributable to a
stem canker.’
Alnus is a circumpolar, dominant, deciduous broadleaf
shrub in the boreal biome. It is the key genus responsible
for nitrogen (N) fixation in floodplains of interior Alaska
(Ruess et al., 2009). Alnus is an important food source for
insect herbivores, microtines, rodents and ungulates.
Warming at high latitudes, especially interior continental
regions, has been twofold the global average (IPCC, 2007).
Increased temperatures (both winter and summer) will favor
an increase in deciduous woody species, but will probably
increase plant drought stress (Chapin et al., 2010).
2011 The Author
New Phytologist 2011 New Phytologist Trust