The Plant Cell, May 2013, www.plantcell.org ã 2013 American Society of Plant Biologists. All rights reserved.
TEACHING TOOLS IN PLANT BIOLOGY™: LECTURE NOTES
Plant–Plant Interactions
Plants lack familiar sense organs, such as eyes and ears, and
often mistakenly have been thought to be insensitive. Through-
out much of history, plants were considered to be the passive
subjects of the actions of others, such as pathogens and
herbivores, but the 20th century brought an awareness of the
many ways that plants sense and respond to threats and
opportunities conferred by others. This lecture examines how
plants perceive and respond to other plants, how these plant–
plant interactions affect the growth and productivity of individual
plants, and their broader effects on plant communities. Although
the community-level effects of plant–plant interactions have
been recognized and studied for years, their molecular un-
derpinnings are relatively recent discoveries and continue to be
debated and examined. In this lecture, we will introduce well-
established and more tentative, emerging models of plant–plant
interactions. We start with brief definitions of some key terms.
KEY DEFINITIONS AND CONCEPTS
Phenotypic Plasticity
Phenotypic plasticity is the capacity of an individual (or a geno-
type) to exhibit a range of phenotypes in response to variation in
the environment. It specifically refers to processes that are
selected from alternative choices, based on information per-
ceived. In animals, examples include the production of a defensive
helmet by Daphnia in the presence of predators and temperature-
dependent sex determination in reptiles and fish. When consid-
ering phenotypic plasticity in plants, it is helpful to consider that,
unlike animals, plants continually produce new organs (e.g.,
leaves and roots) and that there is considerable redundancy in
these organs. Examples of phenotypic plasticity are the pro-
liferation of roots at the site of localized nutrient abundance or the
selective senescence and shedding of a shaded branch.
Allometry
Allometry is the study of the relative size, scale, or growth rate of
parts and the consequences of allometric scaling. In many
organisms, the proportions of body parts change during
development. Human babies are born with heads that are
huge relative to their body size. As babies grow, their pro-
portions change due to differences in relative growth rate of their
body parts. A plant’s proportions and activities also change with
growth (ontogenetically), independently of environmental fac-
tors. Studies of phenotypic plasticity must differentiate between
ontogenetic or allometric and environmental contributions.
This is publication number 802 of the Mitrani Department of Desert Ecology.
www.plantcell.org/cgi/doi/10.1105/tpc.113.tt0513
Signals and Cues
Plants sense their environment and neighbors through many cues
and signals. Generally, a distinction can be made between cues and
signals, although the precise definitions are not always agreed upon.
“Signals” serve as intended information broadcasts, while “cues”
are without intention. Information internal to an organism, delivered
by, for example, a hormone, can be assumed to be a signal. External
information might be a cue or a signal. Physical and chemical
information (such as water or a mineral nutrient) is clearly conveyed
by cues. Some biological information might be conveyed by cues
(not intended for broadcast to neighbors) or a signal. Generally,
external biological information should be considered a cue unless
proven otherwise. Ethylene and strigolactones are hormones that
serve as both internal and external information vectors.
Plant Behavior
Plant behavior has been defined as what a plant does in the
course of its lifetime “in response to an event or change in the
environment” (Silvertown and Gordon, 1989). The ability of a
plant to respond to environmental challenges or opportunities is
restricted by its reduced mobility compared with animals, and
so much of what we define as plant behavior is necessarily
limited to developmental, growth, and physiological responses.
A familiar example of a plant behavior is the phototropic cur-
vature of a plant toward a light source, first recorded by
Theophrastus (371 to 287 BC), the so-called father of botany.
Physiological behaviors can be immediate and short term, such
as a change in the expression of a nutrient transporter gene or
pathogen response gene. Morphological, growth-based behav-
iors are slower to take effect and are more permanent. Growth
provides costs as well as opportunities. Allocating resources to
one organ means less is available to another, and retreating from
an already grown organ might have substantial costs. Optimal
plant behavior also requires the integration of information about
the spatial and temporal scales and gradients of environmental
conditions. For example, is a change in the light intensity in-
dicative of a shading tree or a cloud or bird passing overhead?
Is the concentration of a nutrient in the soil increasing or de-
creasing relative to the direction of root growth? Because most
responses, especially those that involve growth, require time, the
functional outcomes of any response will only materialize in the
future. Accordingly, plants are selected to respond not only to
their current environment but also to cues and signals that contain
sufficiently reliable information about their future environment.
Case Study: Heterophylly and Leaf Plasticity in Response
to Submergence
Semiaquatic plants often can produce two or more forms of leaf,
which are determined by the levels of submergence. Frequently,
2 The Plant Cell
the leaves that form underwater are thinner, sometimes elon-
gated, and do not produce cuticles or stomata. Heterophylly in
response to submergence occurs in a wide range of plants,
suggesting convergent evolution. The hormone abscisic acid
and blue light are signals and cues for the aerial leaf form in
many plants. As with all plastic responses, not every genotype is
similarly plastic, and the degree of plasticity of the submergence
response tends to vary with the susceptibility of the plant’s
natural environment to flooding.
COMPETITION FOR LIGHT
Many of life’s most intriguing behaviors arise due to competition.
As Charles Darwin pointed out, organisms that are the most similar
and “fill nearly the same place in the economy of nature” are also
the most competitive. For example, you compete more with your
siblings and classmates than you do with your cat or your teacher.
Because most plants have the same basic needs for water, space,
and a substrate for growth, mineral nutrients, and light, the com-
petition for these resources can be intense (although, as dis-
cussed later, competition is not always necessary). Plants respond
directly to these nutrients and to competing plants, which they
perceive through cues that include nutrient gradients and changes
in the light environment. Responses to competition can include
avoiding competitive environments, tolerating the competitor, or
aggressively confronting the competitor (i.e., fighting back).
With a very few exceptions, plants absolutely require light
energy to drive photosynthesis and fuel all of the plant’s ener-
getic needs. Photoreceptors enable plants to monitor their light
environment, to gauge and differentiate to what extent they are
shaded by other plants or by inanimate objects, and to antici-
pate imminent shading. Some plants respond to vegetative
shading through stem elongation to reach above the shading
neighbor or growing away from the shade. This common and well-
known response, often called the shade avoidance syndrome, is
a developmental scheme that is both an avoidance strategy and
also a confrontational strategy; plants that succeed in shooting up
above their neighbors often end up winning the battle for light.
Other plants do not compete for light but are adapted to tolerate
shade and thrive in low-light conditions. However, even understory
plants compete among themselves for the available light and thus
are expected to be responsive to similar-sized neighbors but not to
very tall canopy trees they have no chance of overcoming.
Light Perception: Photoreceptors Sense Light Intensity
and Spectral Quality
Plants, like animals, have several photoreceptors that are
sensitive to light quality (wavelength or color) and intensity.
Visible light comprises photons with a wavelength range from
;390 to 760 nm. The energy of a photon is inversely correlated
with its wavelength, so per-quantum energy drops off propor-
tionally with increasing wavelength. Photons of short, UV wave-
lengths carry sufficient energy to damage DNA, whereas long-
wavelength infrared light is merely warming. All land plants have
similar photosynthetic machinery that can use photons with
wavelengths of 400 to 700 nm, known as photosynthetically
active radiation (PAR). Longer wavelength photons pass through
the leaf or are reflected off of it. Thus, light that passes through
or reflects off a leaf is depleted in PAR (,700 nm) and is
relatively rich in far-red light (.700 nm) compared with sunlight.
Phytochromes are a group of photoreceptors that detect red
and far-red light and are particularly important for the optimi-
zation of photosynthesis, perception of day length, and the
perception of other plants. Phytochromes detect photons on
both sides of the boundary between PAR and far-red light.
They do this by existing in two alternative conformations that
preferentially absorb photons at ;660 or 730 nm. When activated
by red photons, phytochromes change their conformation into
a form that is capable of absorbing far-red light, known as Pfr.
When Pfr absorbs far-red light, it switches back to a conformation
known as Pr that can absorb red light. Thus, phytochromes are
switches that toggle back and forth, like a light switch. In a cell
that contains hundreds of thousands of phytochrome molecules,
the proportions of both forms will depend on the relative
abundance of red and far-red photons, in other words, the red
to far-red (R:FR) ratio. The Pfr form initiates downstream
responses, such as chlorophyll accumulation and leaf expansion,
through changes in gene expression and hormone responses.
Plants have additional photoreceptors that are sensitive to blue
and UV light (cryptochromes, phototropins, and UV receptors),
which also contribute to the regulation of plant light responses.
Through its photoreceptors, a plant perceives information
about its environment. At the crudest level, the plant perceives
the relative quantity light of different wavelengths, but there is
considerable data to indicate that the information perceived is
much richer. For example, photoreceptors are present through-
out the plant body, allowing the plant to sense the quantity and
quality of light coming from different directions, as well as spatial
and temporal light gradients. Light perceived by a plant from
different directions conveys valuable information about the
presence and location of neighboring plants, even when those
neighbors are still small and remote.
Shade Avoidance Syndrome
One set of responses to vegetative shading or to the possibility of
future shading is the shade avoidance syndrome. These re-
sponses affect many aspects of plant behavior and can include an
inhibition or delay of seed germination, increased stem and leaf
elongation, a more vertical orientation of the leaves (hyponasty),
a decreased number of branches (i.e., stronger apical domi-
nance), and accelerated flowering. The elongation responses may
enable the plant to confront a competing plant and increase its
chances to rise above it. Beyond light cues, there is now evidence
that touch and volatile compounds, including the hormone
ethylene, serve as anticipatory cues that contribute to shade
avoidance, at least in Arabidopsis thaliana.
Case Study: Portulaca oleracea
Shade avoidance does not necessarily involve upwards growth.
Plants with a prostrate growth habit can sense and anticipate
shading and orient their direction of growth to avoid it. As an

example, the spreading succulent P. oleracea grows and
branches in a way that minimizes both self-shading and
anticipated shade of neighboring plants, and the growth pattern
is attributed to the R:FR ratio of the light reflected by neighbors
and other parts of the same plant. When subjecting young
P. oleracea seedlings to contrasting light cues, they become
recumbent and grow away from sources of far-red light even
when that means growing toward a region of less photosynthetic
light. In other words, for young seedlings, low R:FR sunlight,
a cue for future competition for light, is a strong deterrent. The
plant chooses to forgo more light now to increase its potential to
receive more light during the rest of its life.
Shade Tolerance
Plants respond in different ways to vegetative shading, and
many do not respond through a shade avoidance response.
Some species, known as shade-tolerant species, have evolved
to thrive in the low-light environment beneath the forest canopy;
the amount of PAR at ground level can be as little as 2% of that
that hits the top of the overlying forest canopy. Although shade
tolerance can take many forms, a few characteristics are fre-
quently found among these species. Note that some of these
features can be adopted by sun-loving plants growing in the
shade, but others are restricted to shade-tolerant plants.
A fundamental requirement for survival in dim light is the ability
to maximize the net rate of energy gain. Often, this means that
the leaves of shade-tolerant plants are relatively thinner but with
a larger area for light capture than those of sun-loving plants.
Shade leaves also usually have a higher ratio of chlorophyll b to
chlorophyll a, as a consequence of an increased size of light-
harvesting antenna complexes relative to reaction centers.
Similarly, compared with sun-loving plants, shade-tolerant
plants have a lower stomatal density and lower abundance
of the carbon-fixing enzyme ribulose-1,5-bisphosphate
carboxylase/oxygenase in the chloroplasts. Taken together,
these features mean that in shade-tolerant plants, the rate of
photosynthesis saturates at a lower light intensity (the light
saturation point is lower) than in sun-loving plants. At the same
time, shade-tolerant plants typically have a higher ratio of
photosynthetic tissues (e.g., leaves) to nonphotosynthetic
tissues (e.g., twigs, branches, and roots), which contributes to
a lower rate of respiration in the dark per unit leaf area in shade
leaves. As a consequence of this, the light compensation point
(light intensity at which CO2 uptake 5 CO2 evolution) is lower in
shade-tolerant plants. Collectively, these morphological and
physiological traits enhance carbon accumulation in low-light
conditions.
Optimization of carbon gain alone does not fully explain the
basis of shade tolerance; responses to abiotic and biotic
stresses have to be considered as well. Typically, compared
with sun-loving plants, shade-tolerant plants have longer-lived
leaves and invest more energy into protecting their leaves by
increasing expenditures into defense against herbivores and
pathogens. Furthermore, mechanisms of shade tolerance are
constrained by the availability of water and the length of the
growing season. For example, morphological adaptions to
shade (large leaves) and drought (large root systems) might be
May 2013 3
achievable in a tropical plant, with a year-round growing season,
but not in a temperate plant that only achieves a positive carbon
balance during a few months of the year.
Finally, shade-tolerant species typically show a reduced stem
elongation response to vegetative shading compared with sun-
loving plants; nevertheless, these shade-tolerant plants might
compete with their similar-sized understory neighbors. In terms
of competitive behaviors, plants of shaded habitats often tolerate
low light and avoid confrontational stem elongation responses that
are likely to be futile, sun-loving plants tend to be confrontational,
and plants that are typical to sparse, competition-free stands tend
to avoid confrontation.
The light environment of plants is extremely information-rich,
and plants are likely to perceive subtle information about the
position, height, and growth rates of their neighbors through
absolute amounts of light of different wavelengths, the angle of
incidence of the light, light gradients, and time-of-day light
information, perceived through interactions with the biological
clock. Strong shade at midday followed by more light in the late
afternoon might be the result of shading from a much taller tree
and thus trigger an adaptation to enhance light collection within
the understory rather than confrontational growth elongation. In
addition, a plant might be more responsive to a vertical light
gradient, where a plant encounters more light as it grows
upwards and which indicates light competition by plants of
similar stature than to homogenous shade, in which light intensity
does not increase with increasing height and which indicates
much taller and, thus, unbeatable neighbors.
Of course, as described below, the information conveyed by
the light environment is augmented by chemical and other cues
produced and affected by neighbors. The more we learn about
the interactions between plants, the more sophisticated we
recognize them to be. Is it any surprise that organisms that have
competed with each other for space and resources for more than
400 million years are pretty good at sizing up their competitors?
Germination Plasticity
The global dominance of seed plants is attributable to their
ability to wait out hard times as stable, dormant seeds. One of
the most important choices a plant makes is when to germinate
and shift from a safe to a vulnerable state. Getting the timing
right means the difference between success (surviving to re-
produce) and total failure (dying before reaching reproductive
age). Although they appear inert, seeds are extremely sensitive
to their external environment. Some of the cues that seeds
are responsive to include light (with far-red light strongly
suppressing the germination of seeds of many sun-loving
plants), moisture, heat, smoke, etc.
Some but not all seeds require light for germination. Classic
studies of seed germination, by Flint and McAlister (1935 and
1937), subsequently reproduced by Borthwick et al. (1952),
used a light-sensitive variety of lettuce (Lactuca sativa). Their
experiments showed that white light or red light stimulates
germination but that far-red light is strongly inhibitory. These
studies further demonstrated that the germination response was
photoreversible, with far-red and red light reversing each other’s
4 The Plant Cell
effects, an early and clear demonstration of the nature of phy-
tochrome. In such light-sensitive seeds, exposure to vegetative
shading promotes a continued state of dormancy, avoiding
a competitive environment.
Smoke and heat are other cues that can promote germination.
Fire-responsive plants, including many endemic to the fire-
prone regions of Australia, germinate or sprout following fire.
Fires can open the canopy to reduce the competition for light but
also generally result in improved growth conditions. Fires
reintroduce nutrients into the soil, so fire-induced germination
helps plants avoid competition for nutrients as well as light. In
some cases, the response is to the heat of the fire, which can
remove germination inhibitory compounds from the soil. Re-
cently, a family of germination-promoting compounds called
karrikins was identified from the smoke of burned plant ma-
terials. (The name karrikin is derived from karrik, a word for
smoke used by a group of Aboriginal people of Australia.)
Karrikins are stable in soil and very potent promoters of ger-
mination of many plant species, not only of fire-adapted species.
Interestingly, karrikins and their signaling pathway closely re-
semble strigolactones and their signaling pathway. Strigolactones
are plant hormones that also have additional roles in plant cueing
and signaling between organisms.
Serotiny is another trait that allows plants to exploit postfire
opportunities. Prevalent in many gymnosperms and some an-
giosperms, serotiny is a condition in which seeds are stored for
prolonged periods in closed cones or fruiting structures, often in
the canopy (rather than the soil). Serotinous structures remain
closed with encapsulated seeds protected from predators until
the heat of a fire opens them, sometimes by melting a resinous
coating. Some other fire-responsive plants are induced to
sprout or flower following fire, including the fire lily (Cyrthanthus
ventricosus), which survives as an underground bulb and only
flowers after a fire. Ethylene released from burning material may
contribute to this response. Fire thus provides many cues that
inform plants about the potential release from competition from
other plants. This leads us to the question of what happens if the
strongest competition comes from the plant itself, a phenome-
non known as somatic competition.
Somatic Competition
The modular nature of plants means that they can produce many
redundantly functioning organs. Growth often includes the ad-
dition of more leaves, branches, roots, flowers, and fruits, as
well as the expensive growth of any or all of them. More often
than not, this growth redundancy results in somatic competition
among organs of the same plant. That is, one branch or leaf
might shade another from the same plant. Nevertheless, the
outcome of somatic competition is increased performance of
the entire plant. The plant can explore many microenvironments
and allocate more resources to organs that grow in the most
favorable conditions. For example, a successful branch will not
only grow faster than a less successful branch on the same
plant, it will also induce the differentiation of more vascular
strands toward itself at the expense of vascular connections
to other, less successful (i.e., shaded), branches on the same
plant. Ultimately, the outcompeted branch may be shed, a
phenomenon made apparent by the absence of branches at the
base of the trunk of any tree, especially tall trees growing in
dense stands. The integration of cues and signals that leads
to some organs “winning” and others “losing” is referred to
as correlative inhibition. Somatic competition also occurs in the
root system and the reproductive organs, in which limited
resources are allocated only to the best-performing flowers and
seeds.
Clearly, light and photosynthate contribute to the dominance
of one branch over another, but plasticity is also under the
control of endogenous signals. Numerous studies of small,
short-lived plants (including Pisum and Arabidopsis) indicate
that the control of bud outgrowth is under hormonal control. The
axillary bud that forms in each phytomer may or may not grow
out. Apical dominance is the suppression of lateral bud
outgrowth by the flow of auxin from the shoot apex. The
hormones auxin, cytokinin, and strigolactones as well as nutrient
availability all contribute to apical dominance and correlative
inhibition.
Case Study: Two-Shoot Peas
In a classic paper by Snow (1931), the interactions between
two shoots on a single plant were investigated. He germinated
peas and then decapitated them. Two side branches initiated
from the cotyledonary axillary buds, making an ideal system in
which to investigate somatic competition. Snow showed that
when one of the two shoots was cut off and the other was
growing in the dark, the darkened shoot could survive and
further develop using the nutrients reserves in the cotyledons.
However, when one shoot was placed in the dark and the
other in the light, the shoot in the dark died. Nutrients were
preferentially allocated to the more successful shoot, at the
expense of the weaker shoot. The results of Snow’s studies
demonstrated that the growth of each shoot is not independent
but that they are correlated with each other: that allocation of
resources depended on both local conditions under which
each shoot developed but also on the success of other shoots
on the same plant.
BELOWGROUND COMPETITION
Root Plasticity and Behavior: Nutrient Foraging
In most environments, plant growth is limited by nutrient avail-
ability. Vascular plants take up nutrients usually through their
roots, which forage for nutrients. Foraging behavior includes
changing the rate and direction of growth of individual roots as
well as the timing and positioning of new root initiation and root
hair initiation and root death. Factors that affect root growth and
architecture include the volume of soil, the level and heteroge-
neity of any of at least 20 essential mineral nutrients, water
availabilities, the presence of other roots and organic molecules
produced by other plants, and the presence and activity of
microorganisms (e.g., mycorrhizal fungi, nitrogen-fixing rhizobia,
and various pathogens).

According to the optimal foraging theory, plants will behave in
such a way to maximize their net gain of energy and resources.
When a root encounters a locally rich resource patch, it often
invests resources, through root proliferation or nutrient trans-
porter activity, to increase resource uptake and assimilation. At
the same time, when soil resources are scarcer than light, plants
allocate relatively more of their biomass to their roots; scarce,
widely distributed nutrients force the plant to invest more
resources in the root system to explore a larger soil volume.
Cues that inform root behavior include nutrient availability as
well as other, less well understood cues that indicate the presence
of other roots.
Most plants (;90% of species) can recruit the aid of symbiotic
mycorrhizal fungi for more effective foraging. Under conditions
of nutrient limitation, root-exuded strigolactones are released
into the soil and recruit the fungal partners. The plant provides
the fungi with photosynthate, and the fungi increase the surface
area for nutrient uptake, particularly phosphate. Most legumes
similarly can recruit nitrogen-fixing rhizobia, which provide these
plants with a competitive advantage (at the expense of photosyn-
thate) in nitrogen-limited environments.
Root Plasticity and Behavior: Interactions between Roots
How do roots recognize other roots? Like many questions about
roots, our understanding lags behind our understanding of the
same phenomena in shoots, largely because roots are more
difficult to study. The studies and findings we present here are
intriguing, but in some cases their meanings remain open to
interpretation and ongoing discussions. The story of how roots
perceive and interact with each other is not yet clear.
Competition between Roots of Different Species
and Genotypes
The results of many studies indicate that a competing root can
suppress the growth of another. One mechanism for the
suppression of growth by a competing root is that when two
roots compete for limiting nutrients, their growth rates can be
reduced due to nutrient limitation. An alternative, non-mutually
exclusive mechanism is the production of root-exuded allelo-
chemicals (chemicals that affect others) by one or the other
root.
Many plants are known to produce allelochemicals. These
small molecules can be produced by various tissues and can
affect seed germination as well as root growth. Two of the most
studied allelochemicals are juglone, produced by black walnut
(Juglans nigra), and sorgoleone, produced by sorghum (Sorghum
bicolor). Because of their specificity, several allelochemicals have
been investigated as natural herbicides. For agricultural applica-
tions, allelochemical-producing plants can be desirable crops
because they effectively suppress competing weeds, but they
have to be managed carefully because they also can leave
chemical residues in the soil that affect subsequent crop cycles.
Allelochemicals can act directly or indirectly, through effects
on soil microbes. In the US, the aggressive invasive species
garlic mustard (Alliaria petiolata) produces allelochemicals that
May 2013 5
inhibit mycorrhizal fungi, which most plants rely upon for
efficient nutrient uptake. Like other crucifers, garlic mustard
does not associate with mycorrhizal fungi, so the allelochem-
icals it produces do not affect its own growth. Furthermore, its
impact is much lower in Europe, where it is native, than in the
Americas, suggesting that following their long coevolution, the
European mycorrhizal fungi are less susceptible to it, supporting
the “novel weapon hypothesis” whereby invasive species can
dominate an environment, the species of which haven’t had
enough evolutionary time to evolve mechanisms to deal with the
aggressive traits they bring.
Do Plants Perceive and Discriminate between Self,
Non-Self, and Kin?
Studies in social animals support a role for kin selection and
even seeming altruism in some behaviors, such as the shared
rearing of infants by chimpanzees and elephants or the division
of labor seen in social insects like bees and ants. An unresolved
question in our understanding of plant–plant interactions is to
what extent the relatedness of the competing plants matters.
Although this question remains unanswered, some recent
studies suggest that plants can discriminate between kin and
non-kin, and self and non-self, but how this information is used
is less clear.
In one study, pairs of rice (Oryza sativa) plants of the same or
different genotypes were grown in clear gels and the extent of
overlap between root systems measured. Roots of different
genotypes tended to avoid each other and showed less overlap
than root of the same genotype. This avoidance might arise from
the production of different chemical exudates by roots of
different genotypes.
Another study using peas investigated the responses of plants
to other individuals of the same species and genotype, in an
effort to determine if root foraging might minimize somatic
competition (competition between roots of the same individual).
The results of this study indicated that roots compete more (as
measured by mass and directional growth) with other individuals
than with self. When the connections between the roots of the
same plant were severed, the roots lost some ability to re-
cognize each other as belonging to the same plant/self. A similar
result was found using Buchloe dactyloides. Taken together,
these and other studies suggest that plants can recognize self
and kin, though the precise signaling underlying these phenom-
ena is yet to be revealed.
Case Study: Parasitic Plants
Parasitism can be considered an extreme form of competition.
About 1% of angiosperms have evolved the ability to parasitize
other plants: that is, to penetrate into their tissues and extract
water and nutrients from them. Most parasitic plants are
facultative opportunists, but a few have become completely
dependent on their hosts as nutrient sources. In some tropical
regions, such as the savanna agriculture in Africa, parasitic
plants are major agricultural pests and can impact the food
security of more than 100 million people. Much of the damage is
6 The Plant Cell
caused by parasitic witchweed (Striga spp) and broomrape
(Orobanche spp and Phelipanche spp).
Parasitism is a complex trait that requires specific recognition
of suitable hosts, evasion of their defense responses, and
extraction of nutrients from them. Invasive structures called
haustoria, analogous to those formed by pathogenic oomycetes
and fungi, penetrate the host’s shoot or root and serve as
conduits through which nutrients and water are transferred to
the parasite. Some parasitic plants have evolved a strong de-
pendency on their host, even to the point of losing their ability to
perform photosynthesis, including the loss of many chloroplast-
encoded photosynthetic genes.
Host recognition involves both chemical and tactile cues.
Flavonoids released into the soil by host plants are important
cues for some parasitic plants, as are the strigolactone hor-
mones that were first characterized based on their ability to
promote germination in Striga. Striga parasitism is prevalent in
the low-input, unfertilized fields that are common in parts of Asia
and Africa to a large extent because the nutrient-limited crops
release strigolactones that are signals perceived both by
beneficial mycorrhizal fungi and by parasitic plants. It has
been shown that Striga parasitism is decreased when the crop
plants are provided with exogenous fertilizers or grown with
companion crops that enrich the soil.
COOPERATIVE/FACILITATIVE BEHAVIORS
There is increasing evidence to suggest that the interactions
between plants are not only competitive, but that plants can
benefit each other’s survival, growth, and performance. Positive
interactions can include facilitation, in which both partners
benefit, and commensalism, in which one benefits and the other
neither benefits nor is harmed. Here, we will introduce three
well-documented cases of beneficial interactions in plants: mod-
ulation of the abiotic environment, enhanced nutrient availability,
and stress cueing.
Modulation of the Abiotic Environment
Beneficial associations between plants that help them to
withstand harsh physical environments are widely documented.
These can include acting as wind breaks, increasing the re-
tention of soil moisture, changing the physical characteristics of
soil, increasing soil oxygenation in water-logged environments,
and decreasing soil salinity. Another example comes from nurse
plants, which are adult plants that shelter seedlings as they
establish. As an example, saguaro cactus (Carnegiea gigantean)
seedlings are not very heat or desiccation tolerant but can
survive under the shade of another plant, which is often the palo
verde (Parkinsonia spp). Unfortunately, it is not uncommon for
the saguaro to eventually outcompete its former nurse, in what is
a classic case of succession. Nurse plants can belong to the
same or to different species as the seedlings they protect, can
confer protection from heat, excess radiation, desiccation, and
even herbivory, and often have been described in challenging
arid or alpine environments. The positive impacts that plants can
have on the environment and, thus, other plants may also affect
larger scale, population- and community-level interactions, as
described further below.
Enhanced Nutrient Availability
Although all plants have the same basic requirements, some are
better at meeting these needs than others. In such cases,
different plants can benefit from the strengths of others. In
agroecosystems, facilitations can result in greater yields when
two crops are grown together (intercropping) than when either
species is grown in monoculture. Legumes are known to in-
crease the availability of fixed nitrogen for intercropped partner
plants. They may also indirectly increase the availability of
phosphorous for those plants, through soil acidification. Inter-
cropping may also enhance the availability of minerals such as
calcium, iron, nitrogen, and water through a process known as
hydraulic lift, in which a deep-rooted species bring water up
toward the surface where it can be used by a shallow-rooted
species. Indirect facilitation can occur through effects on rhizo-
sphere microorganisms or through shared mycorrhizal net-
works. A recent study showed that a C4 plant, Sorghum, which
assimilates carbon very efficiently, provides carbohydrate to
a common mycorrhizal network that greatly facilitates the
growth of the intercropped flax, a C3 plant. Thus, in some of
these systems, the community benefits from each according to
its abilities. Carbohydrate sharing also occurs through naturally
occurring root grafts, which can provide life support to a plant
whose ability to assimilate carbohydrates is limited by shading
or logging; at the same time, it can present a significant burden
to the donor plant.
Case Study: Community-Level Effects of Phenotypic
Plasticity in Rooting of Quercus douglassi
How do phenotypic plasticity and facilitative interactions affect
plant communities? Plant ecologists have documented a wealth
of community-level interactions between plants, and we urge
the reader to explore this topic further. Here, we mention one
study that looked at the blue oak Q. douglassi. The architecture
of the oak’s roots shows a high degree of plasticity, and
depending on whether they can access deep water reserves,
they can vary root density near the soil surface. Trees that
produced a large biomass of shallow roots competed more
effectively with nearby plants, reducing the biomass of un-
derstory plants by about half compared with nearby open
grasslands. By contrast, trees with deeper roots had a facilitative
effect on nearby understory plants that had about twice the
biomass compared with plants in the nearby open grassland.
Thus, through phenotypic plasticity, environmental heterogene-
ity at the scale of the individual tree can be translated into higher
level effects on populations and communities.
Stress Cues
Many animals produce alarm signals, which warn their kin, clan,
troop, or flock of danger, which is usually a predator. In some

cases, the alarm conveys information about a predator, such as
whether it is threatening from above or below (e.g., a hawk or
a snake). There is growing evidence that plants also produce
alarm signals or cues through the release of volatile chemicals.
Whether these have evolved to elicit responses in the emitting
plant itself or in other individuals remains an open question, but it
is clear that plants can eavesdrop on each other and respond to
the cues they perceive. Some of these compounds may have
evolved primarily to convey information to herbivores and/or the
enemies of the herbivores. As examples, wild potato (Solanum
berthaultii) can produce an aphid alarm hormone that scares
away herbivorous aphids, and many plants respond to herbivory
by producing volatile compounds that attract parasitoid or
predatory arthropods.
Evidence that plants can perceive and respond to chemicals
released by others comes from many growth chamber and field
studies. Early studies were criticized as being unrealistic, but
more recently there is accumulating evidence that plant–plant
communication occurs in natural settings. A now classic study
compared tobacco (Nicotiana attenuata) plants near sagebrush
(Artemisia tridentata) that had been mechanically wounded
(clipped) or not. The tobacco near the clipped sagebrush showed
an elevated level of the antinutritive polyphenol oxidase and a
lower level of herbivory than those near the unclipped sagebrush
plants, indicating that some information had been conveyed from
the sagebrush to the tobacco.
Since this landmark study, much effort has gone into identifying
the components of interplant cues, their stability once released
from the emitting plant, whether they convey specific information,
how far they travel, what plants perceive them, and how the
information is recognized and transduced. There is good evidence
to support information-carrying roles for the volatiles methyl
jasmonate, methacrolein, and trans-2-hexenal. Mounting a full
defensive response involves costs and reduced growth rate.
Plants receiving these cues don’t activate a full antiherbivore
defense response, but instead become primed (i.e., increase their
readiness to more readily respond to future attack). Priming
seems to involve the accumulation of signaling intermediates that
enable the plant to respond faster and more vigorously should
they themselves become infested with pests in the future.
Plant production of volatile compounds can benefit the emitting
plant directly by acting as a systemic priming signal for distant or
disconnected tissues. The emitting plant can also benefit from the
enhanced resistance of its neighbors if this leads to a local
decrease in pest or pathogen activity, but only if these benefits are
greater than the cost of helping potential neighboring competi-
tors. Are these stress-induced volatiles cues, or are they signals,
released with the intention of conveying information to others?
Along the same lines, there is some evidence that plants are more
perceptive to cues from kin, but how universal and specific these
stress cues are remains an open question.
Case Study: Communication of Drought Stress
Do plants communicate other types of stress? Recent data
suggest so. To investigate whether drought cues can move from
plant-to-plant, two-root plants were planted such that some
May 2013 7
shared the soil with a drought-stressed plant and others did not.
Following drought stress of a single induced plant, the width of
the stomatal pore decreased in both the stressed plant and the
plants that shared soil with the induced plant, suggesting that
they were anticipating drought. Interestingly, the stress cues
seem to be relayed even by unstressed plants via the root
system. Plants that shared no root connections to the stressed
plant showed no response, indicating that the signal is not likely
to be a shoot-emitted volatile compound such as those involved
in herbivore warning but rather, yet unidentified, root exudates.
PUTTING KNOWLEDGE TO WORK
Far from an esoteric pursuit, understanding the interactions
between plants could have enormous value for improving the
way that humans interact with and take advantage of plants. As
examples, we will briefly describe three applications: invasive
species mitigation, intercropped and allelopathic crop plants,
and exploiting plastic responses to light quality.
Invasive Species Mitigation
Biological invasions are an important cause of global biodiversity
loss. Some of the most economically important invasive species
today are water hyacinth (Eichhornia crassipes), kudzu (Pueraria
lobata), Japanese knotweed (Fallopia japonica), leafy spurge
(Euphorbia esula), giant hogweed (Heracleum mantegazzianum),
and mile-a-minute weed (Polygonum perfoliatum). Each is
a fascinating tale of good intentions and mistakes. Each also
provides vital information as we try to avoid introducing plants into
environments in which they will become pests. It is estimated that
;1 in 10 species moved into a new environment will survive to
reproduce in it, and 1 in 10 of those might become pests (see
Richardson and Pysek [2006] for the caveats). Many of those that
become pests are armed with novel chemical weapons, such as
an allelochemical that attacks other plants, chemicals that affect
the mycorrhizal fungi needed by the native plants, or a chemical
deterrent that protects the invader from herbivores or pathogens.
Many invasive species have greater phenotypic plasticity than the
natives they are displacing, but this is not a hard-and-fast
requirement for invasiveness. Besides this, small seeds, a short
generation time, and large numbers of seeds produced are
frequently associated with invasiveness, but none are require-
ments. Therefore, it is difficult to identify and anticipate potential
problems. However, there is an increased tendency for alien
species to become pests in disturbed environments, particularly
those in which light and/or nutrient resources are abundant, such
as deforested regions and lands downstream of fertilized fields.
These correlations can only remind us to try to tread lightly in our
actions toward the natural environment.
Case Study: Japanese Knotweed, from Prize
Winner to Pariah
Japanese knotweed and its hybrid Fallopia 3 bohemica
(Bohemian knotweed) is listed by the World Conservation Union
8 The Plant Cell
as one of the 100 most invasive species. It was widely distributed
as a prizewinning ornamental plant in the mid-19th century, but
now is a serious pest. It outcompetes native plants partially through
the production of allelochemicals. It grows from underground
rhizomes, so regenerates quickly, making its removal difficult.
Millions of dollars are spent annually on control efforts, but it
continues to spread. Although allelochemicals produced by
Japanese knotweed have not been identified yet, a recent study
showed that their harm could be mitigated by the presence of
activated charcoal in the soil, which adsorbs and neutralizes the
harmful chemicals. Another study found a way to fight fire with fire;
in other words, to use an allelochemical-producing plant bog
myrtle (Myrica gale) as a biocontrol agent with which to inhibit the
growth of Japanese knotweed. Other studies have shown that
knotweed exhibits highly plastic responses to salt, which is thought
to contribute to its competitive success in salty environments.
Case Study: Backfiring Biocontrol of Invasive Knapweed?
Spotted knapweed (Centaurea stobe ssp micranthos, also
known as Centaurea maculosa) is native to Europe and was
introduced to North America in the 1890s. It is a noxious weed
that competes very effectively with native plants and has ruined
millions of acres of rangeland and native habitat throughout
the western US and Canada. Biological control efforts, using
herbivores imported from Europe, were started in the 1970s,
with mixed results. In some studies, the negative effects on
native plants were greater in the presence of the herbivore-
infested knapweed than the uninfested knapweed. Possibly,
herbivory induces defensive allelochemicals in the knapweed
that negatively affect native plants or beneficial soil microbes.
Case Studies: Intercropping, Crop Rotation,
and Crop Allelopathy
Often, crop production can be enhanced by growing two or
more crops in the same field at the same time (intercropping) or
in alternating years (crop rotation). Yield gains occur when the
crops are selected so that they facilitate each other’s growth,
and competition is minimized. A familiar example is the in-
tercropping of maize (Zea mays) and bean (Phaseolus vulgaris),
or maize, bean, and Cucurbita spp, or squash (which have been
referred to as the three sisters). This system of agriculture has
been practiced since ancient times, probably first in Mexico
where maize was domesticated. Maize provides a structure for
the climbing bean vines, beans are nitrogen-fixing legumes that
increase the availability of nitrogen to other crops, and squash’s
large leaves growing near the ground may conserve soil
moisture and suppress weeds. Legumes are also beneficial
when grown in crop rotation, as the nutritional benefits they
confer persist into the next growing season. The three plants
have complementary shoot architectures, with maize being very
tall, bean having small leaves that fit between the gaps of the
maize leaves, and squash producing large leaves near ground
leave. In addition, a recent study found that the roots systems of
legumes and maize are complementary in distribution, which
minimizes their competition belowground.
Additional successful intercropping strategies have been
identified more recently by examining the needs of the farmers
as well as the needs and behaviors of the plants. A nice example
is the push-pull system developed to reduce the impact of stem
borer caterpillars on maize. In this system, the herbivores
are pushed away from the crops by an intercropped plant,
the legume Desmodium uncinatum, which produces repellent
volatiles. The herbivores are pulled toward Napier grass
(Pennisetum purpureum) planted at the perimeter of the field. An
additional benefit of this system is that D. uncinatum also
produces allelochemicals that interfere with Striga parasitism,
protecting the crop from yet another pest. By intercropping, the
farmer greatly increases the maize yield by minimizing herbivory
and parasitism and also produces a nitrogen-rich legume crop
as food for animals.
In Uganda, farmers have found that their coffee yields are
improved when they are intercropped with banana trees, which
provide some shade for the coffee plants. A particular benefit for
the farmer is that the same land can produce a cash crop
(coffee) and a food crop (banana), thus enhancing the farmer’s
food security. Neither coffee nor banana is indigenous to
Uganda, so this successful intercropping strategy could never
have occurred without the input from humans.
Several cereals, including sorghum (Sorghum bicolor), wheat
(Triticum aestivum), barley (Hordeum vulgare), oat (Avena sativa),
and rice, are known to produce allelochemicals that suppress
the growth of other plants. Efforts are underway to introduce
these traits into cultivated varieties of these crop plants, which
could reduce the need for chemical herbicide application and
mechanical weed removal. Traditional and molecular breeding
methods are being used. As an example, the biochemical pathway
for the synthesis of an allelochemical from rice, momilactone B,
has been identified, providing a molecular target for breeding and
metabolic engineering studies.
Case Study: Manipulating the Light Environment for
Increased Productivity
Understanding how plants respond to light intensity, quality, and
gradients will provide us with opportunities to exploit these
responses to alter their growth patterns and productivity.
Greenhouses can be covered with colored filters to alter the
spectral qualities of the light for various desired effects. For
example, copper sulfate dyes filter out some red light but
even more far-red light and can lead to a reduction in plant
height or increase the production of axillary buds. Other
filters can preferentially remove red light, leading to an
increase in plant height. When sun-loving plants, such as
tomatoes and roses, were grown under plastic sheeting with
incorporated fluorescent dyes that increased R:FR ratios (by
absorbing green light and emitting red light), the plants
produced more fruits and flowers than control plants grown
under clear covers. Similar results can be obtained using
light-emitting diodes. It is conceivable that greenhouses
could be programmed to provide plants with light custom-
ized to optimize their growth and architecture throughout
development.

SUMMARY AND FUTURE DIRECTIONS
In many respects, the understanding of plant–plant interactions
lags behind our understanding of other plant biotic interactions.
Although phenomena such as the benefits of intercropping and
allelopathy have been recognized for centuries, studies of the
mechanistic bases for competitive and cooperative plant be-
haviors are relatively recent and ongoing efforts. A picture of
plant interactions is emerging that is surprisingly sophisticated,
in which plants perceive their neighbors through light and che-
mical cues, evaluate the extent to which these neighbors pose
a threat, and respond appropriately.
It is likely that our understanding of these sensitive signaling
and response systems can be manipulated to improve crop
yields. For example, rather than manipulating light spectral
qualities through filters, field-grown plants could be manipulated
through an engineered phytochrome that could be induced to
switch between Pr and Pfr forms by exogenous chemical
signals. Thus, optimal architecture for crop production could be
maintained, even in very densely planted fields. Genetically
manipulating the responses of plants to the stress cues emitted
by other plants or artificial preemptive treatments could effectively
increase plants’ tolerance of pests or abiotic stresses.
Advances in metabolomic profiling and genomic and tran-
scriptomic approaches may provide tools with which to de-
cipher plant–plant interactions at the molecular level. We do not
yet fully understand the molecular and genetic mechanisms
underlying phenotypic plasticity nor to what extent epigenetic
genome modifications are involved. Building up a predictive
network from genes and environment through response and
phenotype is important for modeling and managing natural and
agroecosystems. The sustainable intensification of agriculture
is necessary to feed the world’s population while preserving
biodiversity and wilderness environments, but to achieve this
goal scientists need to harness the power of plants to work
with each other and limit their tendencies to act against each
other.
Mary Williams
mwilliams@aspb.org
Features Editor, The Plant Cell
c/o Plant Science Research Group
University of Glasgow
Ariel Novoplansky
anovopla@bgu.ac.il
Mitrani Department of Desert Ecology
Blaustein Institutes for Desert Research,
Ben-Gurion University of the Negev
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