© 2013 American Society of Plant Biologists Plant-plant interactions Photo courtesy of Ronald PierikRonald Pierik

© 2013 American Society of Plant Biologists

Plant-plant interactionsPhoto courtesy of Ronald Pierik

http://www.uu.nl/staff/Rpierik/


Plants sense and respond to other plants植物感知和响应其他植物

Often, but not always, plants compete with each other for limiting resources, such as light and nutrients通常，但不一定是，植物对有限资源是相互竞争的，如光和营养。How do they perceive competitors?他们是如何感知竞争对手的？Are all of their interactions competitive? 所有植物之间的交互作用都是竞争性质的吗？How do interactions between plants affect higher organizational levels (e.g., communities)? 植物之间的相互作用是如何影响更高水平的组织结构的？如群落

Photo credit: Tom Donald

http://www.flickr.com/photos/clearwood/3107589712/in/set-72157626284715720


Outline概要Key definitions and concepts关键的定义和概念Competition竞争•Competition for light 光•Competition belowground地下竞争•Do plants perceive “self” or “kin”?•植物自我和亲属是怎么感知的？

Cooperation / Facilitation协同和促进•Environmental modulation环境的调节•Enhanced nutrient availability提高营养物质的有效性•Stress cues胁迫信号Putting knowledge to work

Photo credit: Mary Williams


Key definitions and concepts

Reprinted by permission from Wiley from Drew, M.C. (1975). Comparison of the effects of a localised supply of phosphate, nitrate and ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol. 75: 479-490. Reprinted from Vandenbussche, F., et al. (2005). Reaching out of the shade. Curr. Opin. Plant Biol. 8: 462-468 with permission from Elsevier, Reprinted from Sultan, S.E. (2000). Phenotypic plasticity for plant development, function and life history. Trends Plant Sci. 5: 537-542 with permission from Elsevier. See also Bradshaw, A. D. (1965). Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 13: 115–155.

The capacity of an individual (or a genotype) to exhibit a range of phenotypes in response to variation in the environment 个人的能力 ,表现出一系列的表型 ,以应对环境的变化

Phenotypic plasticity 表型可塑性

Polygonum lapathifolium酸膜

Low light光 High light

Nicotiana tabacum烟

Low Red: 远红外的比率

High Red: Far-red ratio

Low phosphate

Low phosphate

High phosphate

P水平

http://onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.1975.tb01409.x/abstract

http://www.sciencedirect.com/science/article/pii/S136952660500097X

http://www.sciencedirect.com/science/article/pii/S1360138500017970

http://www.sciencedirect.com/science/article/pii/S0065266008600486


Phenotypic plasticity in plants植物的表型可塑性

Reprinted by permission from Wiley from Drew, M.C. (1975). Comparison of the effects of a localised supply of phosphate, nitrate and ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol. 75: 479-490. Photo credit Michael Clayton.

Root plasticity in response to localized nutrient availability

Shoot plasticity in response to light光

根可塑性响应局部营养的可用性

http://onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.1975.tb01409.x/abstract

http://botit.botany.wisc.edu/Resources/Botany/Shoot/Stem/Phototropism/Etiolation.jpg.html


Signals and cues

Signals are generally considered to be an intended information broadcast and can include: hormones, bacterial metabolites, electrical signals, light quality, stress signals

Cues are considered to be without intent and can include:Nutrient resources, water, light

Signals and cues convey information

Semaphores are signals

Odors and light can be cues

See for example, Aphalo, P.J. and Ballare, C.L. (1995). On the importance of information-acquiring systems in plant-plant interactions. Funct. Ecol. 9: 5-14. Aphalo, P.J., Ballaré, C.L. and Scopel, A.L. (1999). Plant-plant signalling, the shade-avoidance response and competition. J. Exp. Bot. 50: 1629-1634. Image from Nesnad.

http://www.jstor.org/discover/10.2307/2390084

http://jxb.oxfordjournals.org/content/50/340/1629.short

http://en.wikipedia.org/wiki/Flag_semaphore


Signals and cues affecting plants

INFORMATION

Internal Signaling

Primary metabolitesHormonesElectrical pulses

ExternalCueing Signaling

Biotic only Abiotic: Physical and chemical environment atmospheric, edaphic.

Biotic: Secretions, exudates, volatiles etc

External cueing: Can be observedExternal signaling: Initially, only a hypothesis. Whether it is adaptive for the emitter as well as the receiver must be determined

Some hormones, such as ethylene and strigolactones, serve as communication vectors both internally and externally


Cues inform decisions about when and how to allocate finite resources

Like a poker player, plants have limited resources. Gambling on a bad hand, or expending resources at the wrong place or time can be a big mistake

Signals and cues indicate the “best bet”

Cues that indicate future conditions and circumstances are particularly important. Plants grow slowly, and can’t run away, so they have to live with the consequences of their behaviors

See for example Shemesh, H, BF Zaitchik, T Acuna, and A Novoplansky (2012) Architectural plasticity in a Mediterranean winter annual. Plant Signal. Behav. 7:492 – 501 and Shemesh, H. and Novoplansky, A. (2012) Branching the risks: architectural plasticity and bet-hedging in Mediterranean annuals. Plant Biol., In press. Photo credit Tom Donald.

http://www.landesbioscience.com/journals/psb/article/19467/

http://www.flickr.com/photos/clearwood/7364969008/sizes/o/in/set-72157626284715720/


Plant behavior

What a plant does in the course of its lifetime, in response to an event or change in the environment

Example: Phototropic curvature towards a light source

Images: Wisconsin fast plants, Tangopaso

http://www.fastplants.org/resources/pauls_sandbox_category_article.php?entry_id=102

http://en.wikipedia.org/wiki/File:Phototropism.jpg


Plant behavior affects morphological and biochemical phenotypes

Shaded

Full sun One of the most studied plastic responses is shade-induced stem elongation

The induction of defense responses to herbivory or pathogens is another type of phenotypic plasticity. For example, herbivore attack can induce the synthesis of an anti-nutritive such as a protease-inhibitor

Franklin, K.A. and Whitelam, G.C. (2005). Phytochromes and shade-avoidance responses in plants. Ann. Bot. 96: 169-175. Ryan, C.A. (1990). Protease inhibitors in plants: Genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 28: 425-449.

Plants can’t run away – they have different forms of behavior

http://aob.oxfordjournals.org/content/96/2/169.short

http://www.annualreviews.org/doi/abs/10.1146/annurev.py.28.090190.002233


Plant behavior is affected by many environmental parameters

Genome and epigenome

Abiotic factors: Light, moisture, nutrients, etc.

Biotic factors: competitorssymbionts, pathogens, herbivores, etc.

Phenotypic outcomes:•Number and length of root and shoot•Number, size and architecture of leaves, branches and lateral roots•Production of metabolites •Etc.

Plant behavior is mediated through phenotypic plasticity


Case study: Plasticity of leaf morphology in aquatic plants

Lin, B.-L. and Yang, W.-J. (1999). Blue light and abscisic acid independently induce heterophyllous switch in Marsilea quadrifolia. Plant Physiol. 119: 429-434.

Submerged leaf phenotype

Many species prone to periodic submergence show phenotypic plasticity of their leaf forms. Submerged leaves are often thinner and without stomata or cuticle.

Aerial leaf phenotype

The hormone ABA is one signal that initiates the switch to the aerial form, and in this plant, Marsilea quadrifolia, blue light is another. The plant was irradiated with blue light at the position indicted by the arrowhead

http://www.plantphysiol.org/content/119/2/429.full


Summary: Behavior is the variable response to the environment

The mechanisms by which plants perceive their environment and integrate information into a behavioral response are not well understood, but under intense investigation

Plant interactions involve perception through cues and signals, and plastic behavioral responses


http://www.flickr.com/photos/clearwood/3107589712/in/set-72157626284715720


Victoria Nuzzo, Natural Area Consultants ; Easy Stock Photos; Hassanali, A., Herren, H., Khan, Z.R., Pickett, J.A. and Woodcock, C.M. (2008). Integrated pest management: the push–pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Phil. Trans. R. Soc. B 363: 611-621 copyright 2008 The Royal Society; Karban, R., Baldwin, I.T., Baxter, K.J., Laue, G. and Felton, G.W. (2000). Communication between plants: Induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia. 125: 66-71. Max Planck Institute for Chemical Ecology, Jena, Germany / Rayko Halitschke.

Plants are affected by each other positively and negatively

Negative effect:

Competition for light

Negative allelopathic effect:

Here, the invasive species Alliaria petiolata (garlic

mustard) suppresses all others

Positive effect: Nutrient sharing and suppression of parasitism

Positive effect: Stress cues

http://www.forestryimages.org/browse/detail.cfm?imgnum=0002039

http://www.easystockphotos.com/settings/meadow.html

http://rstb.royalsocietypublishing.org/content/363/1491/611.full.pdf+html

http://link.springer.com/article/10.1007/PL00008892

http://www.mpg.de/414573/forschungsSchwerpunkt?c=166478


“We can dimly see why the competition should be most severe between allied forms, which fill nearly the same place in the economy of nature...”

Charles Darwin, 1859, On the Origin of Species, Ch 3 Struggle for Existence

With similar needs, competition between plants can be intense

Light information governs shoot phenotype, but also affects root development and interactions

Self-shading Shading by non-self

Nutrient and water distribution and various signals and cues govern root phenotype

Competition and cues from

non-self

Plants compete with themselves and others


Trees growing in forests can grow more than 100 meters high, shading plants below them, including their own offspring

Light can be a limiting resource in many environments

Photos courtesy Ariel Novoplansky


Confront

Avoid

TolerateShade tolerant morphology and physiology

Elongation response, Increased apical dominance

Growing away from competitorsLight- or fire-dependent germination

Responses to shading: confrontation, avoidance, tolerance

Reprinted from Vandenbussche, F., Pierik, R., Millenaar, F.F., Voesenek, L.A.C.J. and Van Der Straeten, D. (2005). Reaching out of the shade. Curr. Opin. Plant Biol. 8: 462-468 with permission from Elsevier, See also Novoplansky, A. (2009) Picking battles wisely: plant behaviour under competition. Plant Cell Environ. 32: 726-741. Photo credits: Lennart Suselbeek; Ariel Novoplansky


Light

Plants perceive light levels and color (or- light quantity and quality)


Detection of light levels and quality

UltravioletShort wavelengthHigh energy

InfraredLong wavelengthLow energy

UV receptor

Blue light receptors

Red / far-red receptors

Plants perceive light through photoreceptors that are sensitive to light of various wavelengths


Absorption spectra for

chlorophyll and accessory pigments

Photosynthetically active radiance

(PAR)

Far- Red light – too little energy for photosynthesis

Phytochrome detects the boundary of photosynthetically active radiance

Phytochrome detects both photosynthetically active red light (660 nm) and photosynthetically inactive far-red (730 nm) light

Cryptochrome detects blue (450 nm) light

Act

ion

sp

ectr

um

fo

r p

ho

tos

ynth

esis


Reprinted by permission from Macmillan Publishers Ltd from Smith, H. (2000). Phytochromes and light signal perception by plants - an emerging synthesis. Nature. 407: 585-591; Adapted from Jaillais, Y. and Chory, J. (2010). Unraveling the paradoxes of plant hormone signaling integration. Nat. Struct. Mol. Biol. 17: 642-645.

A low ratio of red to far-red light is indicative of vegetative shading

Shaded

Full sun

R FR

R FRRed light is depleted as light passes through the canopy

Phytochrome identifies the ratio of Red to Far-red light

(R:FR), an indicator of vegetative shading

PAR

Green and red light are not absorbed by the photosynthetic pigments – they reflect and pass through leaves


Phytochrome’s conformation and absorption spectra “switch”

Phytochrome changes conformation when it absorbs light: Red light converts it to the Pfr form, which mainly absorbs far-red light;Far-red light converts it to the Pr form, which mainly absorbs red light

Reprinted by permission from Macmillan Publishers Ltd from Smith, H. (2000). Phytochromes and light signal perception by plants - an emerging synthesis. Nature. 407: 585-591.


Transduction of light information downstream of photoreceptors

Reprinted from Gommers, C.M.M., Visser, E.J.W., Onge, K.R.S., Voesenek, L.A.C.J. and Pierik, R. (2013). Shade tolerance: when growing tall is not an option. Trends Plant Sci. 18: 65-71 with permission from Elsevier.

Many of the molecular events that contribute to shade avoidance have been elucidated, and include effects on transcription factor activity and hormone levels and responses

Many of the molecular events that contribute to shade avoidance have been elucidated, and include effects on transcription factor activity and hormone levels and responses


Shade avoidance is a collection of responses to vegetative shading

Reprinted from Casal, J.J. (2012) Shade Avoidance. The Arabidopsis Book 10:e0157. doi:10.1199/tab.0157

Light

Vegetative shading

Delayed or suppressed germination

Stem and hypocotyl elongation

Petiole elongation, leaf hyponasty, narrow leaves

Early flowering


From Ballaré, C.L., Scopel, A.L. and Sánchez, R.A. (1990). Far-red radiation reflected from adjacent leaves: An early signal of competition in plant canopies. Science. 247: 329-332. reprinted with permission from AAAS, de Wit, M., Kegge, W., Evers, J.B., Vergeer-van Eijk, M.H., Gankema, P., Voesenek, L.A.C.J. and Pierik, R. (2012). Plant neighbor detection through touching leaf tips precedes phytochrome signals. Proc. Natl. Acad. Sci. USA (2012) 109: 14705-14710.

Plants elongate less when wearing a collar that filters out far-red light reflected from adjacent leaves

Touch is another cue that signals future competition and stimulates elongation

Shade

R FR

Future Shade?


Case study: Portulaca oleracea, light responses in recumbent plant

Reprinted with permission from Novoplansky, A., Cohen, D., and Sachs, T. (1990) How Portulaca seedlings avoid their neighbours. Oecologia 82: 490-493.

Portulaca oleracea grows and branches in a way that minimizes self shading

When lower red/far-red ratios are provided from one direction, the plant grows away, suggesting that phytochrome controls the growth directionality

Low R:FR light

Growth direction; probability


Future shade can be more important than present shade

Grey

Green

Adapted from Novoplansky, A. (1991). Developmental responses of portulaca seedlings to conflicting spectral signals. Oecologia 88: 138-140.

Filters were set up on opposite sides of Portulaca seedlings

One side (grey) transmitted very little photosynthetic light, equally low in R and FR

The other side transmitted and reflected more photosynthetic light but much more far-red than red light

Do the plants grow towards the side with more light now (green) or more light later (grey)? The low R / FR ratio on the “green” side implies the presence of potential competitor…

Little red

Little far-red

Portulaca grows away from far-red light, even when it means that they are growing towards less light

Low R:FR cues indicate the presence of a competitor, so growing away from the direction of such cues might improve the plant’s fitness


Some plants have evolved to tolerate shade – life in the dim lane

Shade-tolerant species are adapted to low light environments

Shade-tolerant species are adapted to low light environments

Photos courtesy Tom Donald and Ariel Novoplansky


Shade tolerance takes many forms

Reprinted with permission from Valladares, F. and Pearcy, R.W. (1998). The functional ecology of shoot architecture in sun and shade plants of Heteromeles arbutifolia M. Roem., a Californian chaparral shrub. Oecologia. 114: 1-10; Coley, P.D. (1988). Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia. 74: 531-536.See also Valladares, F. and Niinemets, Ü. (2008). Shade tolerance, a key plant feature of complex nature and consequences. Annu. Rev. Ecol. Evol. Syst. 39: 237-257 and Gommers, C.M.M., et al. (2013). Shade tolerance: when growing tall is not an option. Trends Plant Sci. 18: 65-71. Photo courtesy of Ronald Pierik

Full sun Shade

Adaptations to maximize light interception: Increased leaf areaLeaves oriented to intercept lightLeaves positioned to minimize overlapHigh chlorophyll b to a content

Growth rate

Def

ense

sLong-lived shade-tolerant plants invest relatively more resources into defenses against herbivores and pathogens

Shade

Sun Reduced stem-elongation response


Energetics of shade tolerance: max. assimilation, min. expenditure

Typically, shade tolerant plants have a lower rate of respiration in the dark, lower light compensation point, and lower light saturation point

Light intensity(μmol/m2/sec)

0

0C

O2 a

ssim

ilatio

n

(μm

ol/m

2/s

ec)

Dark respiration

Lig

ht

com

pen

sati

on

p

oin

t

Shade plant

Sun plant

10

200 400 800

Light saturation point


Light information: Angle, gradients, quality, and time of day

See for example Sellaro, R., Pacín, M. and Casal, J.J. (2012). Diurnal dependence of growth responses to shade in Arabidopsis: Role of hormone, clock, and light signaling. Mol. Plant. 5: 619-628.

Light information is MORE than just quantity and spectrum. It is likely that plants respond to a richer gamut of light cues

Vertical, mid-day shade (possibly low R:FR) might indicate a very tall neighbor – don’t bother trying to catch up!

Horizontal and late-day low R:FR cues might indicate similarly-sized neighbors – go for it!


Germination plasticity: light and other cues for seed germination

Photo credits: Forest & Kim Starr, Starr Environmental; Howard F. Schwartz, Colorado State University, Bugwood.org

One of the most

important decisions a plant makes is when to germinate

Many seeds germinate in response to white or red light, but far-red light is inhibitory

R FR


Fire (heat and smoke) can promote seed germination

Image sources: pfern, Hesperian, © Kurt Stueber, 2003

Fire stimulates seed release or germination in some plants

Some cones and seed pods are fire-serotinous, opening in response to fire

Banskia spp, before and after fire


Karrikins are germination-promoting compounds found in smoke

Reprinted from Chiwocha, S.D.S., Dixon, K.W., Flematti, G.R., Ghisalberti, E.L., Merritt, D.J., Nelson, D.C., Riseborough, J.-A.M., Smith, S.M. and Stevens, J.C. (2009). Karrikins: A new family of plant growth regulators in smoke. Plant Science. 177: 252-256 with permission from Elsevier, and see also Flematti, G. R., et al., (2004). A compound from smoke that promotes seed germination. Science 305: 977.

Fire-induced germination lets seedlings become established with less competition from taller plants.

Karrikins are cues from smoke that promote germination.

However, following a fire, there can be increased competition between similarly-sized seedlings….


Plants produce many redundant organs that compete with each other

Somatic competition can increase plant performance by putting resources into more successful organs

See Sachs, T. and A. Novoplansky (1995) Tree form: architecture models do not suffice. Israel J. Plant Sci. 43:203-212; Photos courtesy Ariel Novoplansky.

Somatic competition: When plants compete with themselves

Are these branches shedding as a direct result of them growing in low light ? Or is it a result of competition with other, more successful branches on the same tree?


Branch autonomy may vary according to circumstances

Adapted from Kawamura, K. (2010). A conceptual framework for the study of modular responses to local environmental heterogeneity within the plant crown and a review of related concepts. Ecological Research. 25: 733-744.

Full sun Full shade Partial shade

L R L R L R

Gro

wth

rat

e

L R L R L RIndependent Competitive Cooperative

There is experimental evidence to support all three types of responses between shoots: independent, competitive and cooperative


Case study: Two-shoot peas and correlative inhibition

See Novoplansky, A., Cohen, D., and Sachs, T. (1989) Ecological implications of correlative inhibition between plant shoots. Physiol. Plant. 77: 136-140; Snow, R. (1931). Experiments on growth and inhibition. Part II. New phenomona on inhibition. Proc. Roy. Soc. B. 108: 305-316. Sachs, T. and A. Novoplansky (1997) What does a clonal organization suggest concerning clonal plants? in de Kroon, H. and J. van Groenendael (eds.) The Ecology and Evolution of Clonal Growth in Plants, pp. 55-78, SPB Academic Publishing, Leiden, The Netherlands.

Two shoot peasRemoving the shoot from a pea seedling causes two shoots to regenerate – a good system to study somatic competition!

5-day old pea

Shoot removal

5 days

“Two-shoot pea”

Two equal shoots can co-exist, but very often one becomes dominant and the other dies

Why does the smaller shoot die?


Case study: Two-shoot peas and correlative inhibition

Redrawn with permission from Novoplansky, A., Cohen, D., and Sachs, T. (1989) Ecological implications of correlative inhibition between plan shoots. Physiol. Plant. 77: 136-140; Snow, R. (1931). Experiments on growth and inhibition. Part II. New phenomona on inhibition. Proc. Roy. Soc. B. 108: 305-316.

A shoot in the dark can survive 10 days (using nutrient reserves), but in competition with a more successful shoot in the light, the darkened shoot dies. The plant selectively allocates reserves to the stronger shoot….

Model: Resources are allocated to the best option. In A, the best (only) option is the shoot in the dark. In B, resources are allocated to the shoot in the light, at the expense of the other shoot.

A. Dark only:100% survival of dark shoot

B. One dark and one light shoot: 20% survival of dark shoot

A. Dark only B. One dark and one light shoot


Within and between trees, branches in the best conditions prevail

Less successful branches, e.g. shaded by neighbors or self are discriminated against and shed



Summary: Perception of and response to vegetative shading

Light is a resource and also a source of information that affects plant behavior

Adaptive responses to competition for light can be architectural (shoot position, size and number), morphological (stem elongation, increased leaf area), physiological (amount of chlorophyll or Rubisco), etc.

Photo credits: Ariel Novoplansky; Reprinted from Vandenbussche, F., et al. (2005). Reaching out of the shade. Curr. Opin. Plant Biol. 8: 462-468 with permission from Elsevier


Competition belowground: Root growth is extremely plastic

Reprinted by permission from Wiley from Drew, M.C. (1975). Comparison of the effects of a localised supply of phosphate, nitrate and ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol. 75: 479-490.. Reprinted from Bouguyon, E., Gojon, A. and Nacry, P. (2012). Nitrate sensing and signaling in plants. Sem. Cell Devel. Biol. 23: 648-654, with permission from Elsevier. See also Gersani, M. and Sachs, T. (1992). Development correlations between roots in heterogeneous environments. Plant Cell Environ. 15: 463-469.

When soil resources are abundant, plants allocate less biomass to their roots

When nutrient distribution is patchy, roots proliferate in the nutrient rich patches


Competition belowground: Root growth is extremely plastic

Reprinted with permission from Fang, S., Clark, R.T., Zheng, Y., Iyer-Pascuzzi, A.S., Weitz, J.S., Kochian, L.V., Edelsbrunner, H., Liao, H. and Benfey, P.N. (2013). Genotypic recognition and spatial responses by rice roots. Proc. Natl. Acad. Sci. USA 110: 2670-2675. Muller, C.H. (1946) Root development and ecological relations of Guayule. USDA Technical Bulletin 923, see also Schenk et al., 1999, Adv. Ecol. Res 28: 145–180, and Gersani, M. and Sachs, T. (1992). Development correlations between roots in heterogeneous environments. Plant Cell Environ. 15: 463-469.

Roots respond to other roots

Many studies have found that roots have a tendency to grow away from each other

Many studies have found that roots have a tendency to grow away from each other


Confront (overproliferate)

Avoid (underproliferate)

Tolerate

Resource limitation

Root-exuded chemicals

Other

Belowground competition: Cues, signals and responses


Plants compete for nutrients, which are frequently limiting for growth

Fisher, J.B., Badgley, G. and Blyth, E. (2012). Global nutrient limitation in terrestrial vegetation. Global Biogeochemical Cycles. 26: GB3007. Credit: NASA JPL/Caltech.

This map shows the difference between actual vegetation productivity and maximum theoretical productivity based on availability of water and sunlight; the difference is attributed to nutrient limitation


Photo credits: Gerald Holmes, Valent USA Corporation, Ulrike Mathesius, Bugwood.org, Sara Wright, USDA; Kristine Nichols, USDA

Most plants enhance nutrient uptake through associations with mycorrhizal fungi or nitrogen-

fixing bacteria 大多数植物提高养分吸收通过对菌根真菌或固氮细菌Some plantsNitrogen-fixing bacteria

Most plantsMycorrhizal fungi

Extensive fungal surface area facilitates nutrient and water uptakeBacteria in nodules

produce reduce atmospheric nitrogen

Fungus inside plant root


Control roots without contact or with a physical barrier

Plants exposed to the chemical exudates of another root system decreased their rate of root growth

In some cases, roots avoid contact or proximity to other roots

Reprinted with permission from Mahall, B.E. and Callaway, R.M. (1991). Root communication among desert shrubs. Proc. Natl. Acad. Sci. USA 88: 874-876.

How do roots respond to the roots of another plant? Plexiglass boxes were set up to record root responses…


Reprinted from Cahill, J.F., McNickle, G.G., Haag, J.J., Lamb, E.G., Nyanumba, S.M. and St. Clair, C.C. (2010). Plants integrate information about nutrients and neighbors. Science . 328: 1657 with permission from AAAS.

Plants integrate information about nutrients and neighbors

Plants were planted alone or with a neighbor, in uniform soil or soil with nutrient rich patches (shaded bar), and root distribution analyzed

In uniform soil, roots avoided each other

But they proliferate in a nutrient-rich patch, in spite of their neighbor


Many plants make allelochemicals that deter competitors

Allelopathic chemicals (allelochemicals) interfere with growth of nearby plants

Sorgoleone is produced in Sorghum bicolor root hairs and exuded as oily drops. It accumulates in the soil and acts as a pre-emergence herbicide affecting photosynthesis in very young seedlings

Reprinted from Dayan, F.E., Howell, J.L. and Weidenhamer, J.D. (2009). Dynamic root exudation of sorgoleone and its in planta mechanism of action. J. Exp. Bot. 60: 2107-2117 with permission of Oxford University Press; Howard F. Schwartz, Colorado State University.

Juglone is an allelochemical produced by black walnut (Juglans nigra)


Allelochemicals can suppress plant growth directly or indirectly

Reprinted with permission from Bertin, C., Weston, L.A., Huang, T., Jander, G., Owens, T., Meinwald, J. and Schroeder, F.C. (2007). Grass roots chemistry: meta-Tyrosine, an herbicidal nonprotein amino acid. Proc. Natl. Acad. Sci. USA 104: 16964-16969, copyright National Academy of Sciences.; Victoria Nuzzo, Natural Area Consultants, Jil Swearingen, USDI National Park Service, Bugwood.org; See also Callaway, R.M., et al., (2008). Novel weapons: Invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology. 89: 1043-1055.

m-tyrosine is a nonprotein amino acid from fescue (Festuca spp) roots, that

inhibits plant growth directly

Alliaria petiolata (garlic mustard) is an invasive plant in the US that indirectly suppresses plant growth through the inhibition of their mycorrhizal fungal symbionts


Summary: Plants compete belowground

©2011 David Graber

The Monterey manzanita (Arctostaphylos montereyensis) suppresses competitors through allelopathy

Besides resource competition, the best understood form of belowground competition is the production of toxic or inhibitory allelochemicals

Additional cues likely contribute to belowground interactions


Is that me?

Plants can respond differently to self, kin and alien

You seem familiar…

Photo credits: Tom Donald


Do plants respond differently to relatives and unrelated plants?

Reprinted with permission from Fang, S., Clark, R.T., Zheng, Y., Iyer-Pascuzzi, A.S., Weitz, J.S., Kochian, L.V., Edelsbrunner, H., Liao, H. and Benfey, P.N. (2013). Genotypic recognition and spatial responses by rice roots. Proc. Natl. Acad. Sci. USA 110: 2670-2675.

Same genotype: More overlap Different genotype: Less overlap - avoidance

YES- This study showed that roots tend to avoid roots of plants that are not related


Do roots discriminate self from non-self?

Yes, plants discriminate self from non-self. Plant B, competing with non-self, makes ~50% more root mass than plant A, competing only with self

A B

Reprinted with permmission from Falik, O., Reides, P., Gersani, M. and Novoplansky, A. (2003). Self/non-self discrimination in roots. J.Ecology. 91: 525-531. Reprinted with permission from Gruntman, M. and Novoplansky, A. (2004). Physiologically mediated self/non-self discrimination in roots. Proc. Natl. Acad. Sci. USA 101: 3863-3867 copyright National Academy of Sciences USA.

These studies showed more root growth in the presence of “other” than “self”. What cues and signals are involved?

Yes, When cuttings that originate from the very same node are separated, they become progressively alienated from each other and relate to each other as genetically alien plants


S/NS may rely on self recognition, rather than on NS discrimination

Reprinted with permission from Falik, O., Reides, P., Gersani, M. and Novoplansky, A. (2003). Self/non-self discrimination in roots. J. Ecol. 91: 525-531.

INTACT TWINS“Double plants” were produced with two shoots and two roots. Some double plants were split, to make “twins”. Some of the split plants were paired up with an unrelated alien. Does a plant recognize self without a physiological connection?

ALIEN

Split pea “Twins” and alien make more roots than intact peas, indicating that physiological connections are important for recognizing “self”

Split pea “Twins” and alien make more roots than intact peas, indicating that physiological connections are important for recognizing “self”

Spatially, intact peas produced more roots toward nonself than toward self roots. Pairs of severed plants developed similarly towards their neighbors, regardless of whether these neighbors were their own twins or alien


Case study: Parasitic plants are extreme competitors

HeavyModerateLight

Striga asiaticaStriga hermonthica

Adapted from Ejeta, G. and Gressel, J. (eds) (2007) Integrating new technologies for striga control: towards ending the witch-hunt. World Scientific Publishing, Singapore; Image sources: USDA APHIS PPQ Archive, Florida Division of Plant Industry Archive, Dept Agriculture and Consumer Services.

•Parasitic plants cost approximately 10 billion USD in crop losses annually

•They infest major cereal crops including corn, sorghum, millet and rice, in over 70 million hectares

•Food production for 300 million people is affected

•No effective control measure has been developed

Parasitic Striga

infestation


Parasitic plants perceive their hosts through chemical cues

Reprinted from Runyon, J.B., Mescher, M.C. and De Moraes, C.M. (2006). Volatile chemical cues guide host location and host selection by parasitic plants. Science. 313: 1964-1967 with permission from AAAS. Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200 Dörr, I. (1997). How Striga parasitizes its host: a TEM and SEM study. Ann. Bot. 79: 463-472, by permission of Oxford University Press.

Host-exuded strigolactones and flavonoids promote germination and attachment of Striga and other parasitic plants

Host root

Striga

Cuscuta pentagona (dodder) uses tropisms, touch and volatile cues, to locate its hosts


Facilitative behaviors: Plants benefitting from their neighbors

Tempering of harsh abiotic environments

Enhancing nutrient uptake

Stress cues can induce anticipatory responses

Walder, F., Niemann, H., Natarajan, M., Lehmann, M.F., Boller, T. and Wiemken, A. (2012). Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol. 159: 789-797.


Reprinted by permission from Macmillan Publishers Ltd from Callaway, R.M., Brooker, R.W., Choler, P., Kikvidze, Z., Lortie, C.J., Michalet, R., Paolini, L., Pugnaire, F.I., Newingham, B., Aschehoug, E.T., Armas, C., Kikodze, D. and Cook, B.J. (2002). Positive interactions among alpine plants increase with stress. Nature. 417: 844-848.

Benefit from others is commonly higher in harsher environments

In harsher, high-elevation environment, plants whose neighbors were removed fared relatively poorly, indicating that they benefited from their neighbors


Plants can protect others from harsh abiotic and biotic environments

Images used by permission of Lohengrin A. Cavieres, Fernando T. Maestre, Pierre Liancourt, and Georges Kunstler. See Brooker, R.W et al. . (2008). Facilitation in plant communities: the past, the present, and the future. J. Ecol . 96: 18-34,.

High AndesBuffered substrate and air temperature, enhanced soil moisture and nutrient content

Semi-arid plains of SpainProtection from drought

Southern FranceProtection from browsing

Semi arid environment, Jordan Protection from browsing and drought


Plants can benefit from amelioration of abiotic stresses by their

neighbors• Wind breaking• Increased retention of soil

moisture• Improved physical

characteristics of soil • Increased soil

oxygenation in water-logged environments

• Increased nutrients• Decreased evaporation

and soil salinity

Photo credits: Tom Donald, Joy Viola, Northeastern University, Bugwood.org

Palo verde (Parkinsonia spp) can act as a “nurse plant” for saguaro cactus (Carnegiea gigantean). Tiny cactus seedlings need shade to get established. Often, though, the cactus later outcompetes its nurse plant


Intercropping and crop rotation confer many benefits

Different crown heights can

accommodate different light requirements

Different root distributions can minimize competition for nutrients

The total yields of fields grown with two or more species at the time or in alternating years can be higher than the most productive monocultures

Legumes increase

nitrogen content of soil

Ground-hugging plants can suppress weeds

Rotating crops reduces pest populations

See Horton, J.L. and Hart, S.C. (1998). Hydraulic lift: a potentially important ecosystem process. Trends Ecol. Evol. 13: 232-235. Lee, J.-E., Oliveira, R.S., Dawson, T.E. and Fung, I. (2005). Root functioning modifies seasonal climate. Proc. Natl. Acad. Sci. USA. 102: 17576-17581.


Walder, F., Niemann, H., Natarajan, M., Lehmann, M.F., Boller, T. and Wiemken, A. (2012). Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol. 159: 789-797.

A common mycorrhizal network can facilitate resource sharing

Flax SorghumMixed

Intercropping with sorghum drastically enhanced flax’s growth (+46% increase). Nutrient uptake was facilitated via the common mycorrhizal network (CMN)


Case study: Community-level effects of phenotypic plasticity

Republished with permission of Ecological Society of America from Callaway, R.M., Pennings, S.C. and Richards, C.L. (2003). Phenotypic plasticity and interactions among plants. Ecology. 84: 1115-1128; See also Callaway, R.M., Nadkarni, N.M. and Mahall, B.E. (1991). Facilitation and interference of Quercus douglasii on understory productivity in central California. Ecology. 72: 1484-1499.

How does phenotypic plasticity and facilitation affect other community members?

Variation in root architecture affects the plant communities associated withQuercus douglasii; only shallow-rooted trees compete with grasses


Cues from other plants can prime plants for defense or tolerance

Reprinted from Glinwood, R., Ninkovic, V. and Pettersson, J. (2011). Chemical interaction between undamaged plants – Effects on herbivores and natural enemies. Phytochemistry. 72: 1683-1689 with permission from Elsevier. Photo credits: Snowmanradio, Justin Johnsen, D. Gordon E. Robertson

Alarm signals are well described in social animals. Stressed plants may emit cues to which other plants respond Be

prepared

cues

cues


Induction and priming of defense responses

Volatile emission

Stomatal closure

Perception of and responses to stress and stress cues

Mechanical damage

Herbivore-derived chemicals

Pathogens

Drought or UV light

Volatile compounds

Root exudates

Genomic instability

Other?


Sagebrush (Artemisia tridentata)

Wild tobacco (Nicotiana attenuata)

Volatile compounds from damaged plants can initiate defenses in others

Karban, R., Baldwin, I.T., Baxter, K.J., Laue, G. and Felton, G.W. (2000). Communication between plants: Induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia. 125: 66-71. see also Kessler, A., Halitschke, R., Diezel, C. and Baldwin, I. (2006). Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia. 148: 280-292. Photo courtesy Ian Baldwin Copyright Max Planck Institute for Chemical Ecology, Jena, Germany / Rayko Halitschke

When nearby sagebrush was mechanically damaged, wild tobacco increased production of defense compounds (PPO) and suffered less herbivore damage

Volatile compounds emitted by damaged

plants can induce defenses in their

neighbors

Volatile compounds emitted by damaged

plants can induce defenses in their

neighbors

The signal(s) travel through air


What are the active compounds and how far do they spread?

Reprinted from Baldwin, I.T., Halitschke, R., Paschold, A., von Dahl, C.C. and Preston, C.A. (2006). Volatile signaling in plant-plant interactions: "Talking Trees" in the genomics era. Science. 311: 812-815 with permission from AAAS.

methacrolein cis-3-hexenal

MeJA

trans-2-hexenal

cineole


Why do plants emit volatile signals?

Reprinted from Arimura, G.-i., Shiojiri, K., and Karban, R. (2010). Acquired immunity to herbivory and allelopathy caused by airborne plant emissions. Phytochemistry 71: 1642-1649 with permission from Elsevier, see also Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trend Ecol Evol 25: 137–144.

• Volatile signals may have evolved for intra-plant communication

• Having defensive neighbors can enhance the emitter’s fitness

• Some volatiles are also inhibitory allelochemicals that reduce competition

• Some volatiles promote indirect defenses by acting as signals to attract predatory arthropods


Case study: Plants may also communicate drought stress

Drought, high salt

?

Stressed Oblivious

Can other stresses be communicated between plants?Can unstressed plants respond to stress cues emitted from their stressed neighbors?

Novoplansky, A. (2012) Learning plant learning.


Testing for root-to-root and relay communication

Novoplansky, A. (2012) Learning plant learning.


Stress cue moves from the stressed plant via the roots

Stomatal aperture was measured in plants without a soil connection and plants whose roots share soil with the induced (IND) plant

Falik O, Mordoch Y, Quansah L, Fait A, Novoplansky A (2011) Rumor has it…: Relay communication of stress cues in plants. PLoS ONE 6(11): e23625. See also Falik, O., Mordoch, Y., Ben-Natan, D., Vanunu, M., Goldstein, O. and Ariel Novoplansky (2012) Plant responsiveness to root-root communication of stress cues, Ann. Bot., 110: 271-280.

Before treatment all the plants had the same stomatal width

After treatment, stomatal aperture was reduced in plants whose roots were in contact (directly or indirectly) with the stressed plant

No response in plants that did not share their rooting volume


Summary: Cooperative and facilitative behaviors

Plants can benefit from other plants, which can• Modulate the abiotic environment, • Facilitate nutrient uptake, and• Emit cues that prime for stress

Like competition, facilitative encounters occur between and within species



Putting knowledge to work

Water hyacinth (Eichhornia crassipes)

Photo credits: Ted Center, USDA; William M. Ciesla, Forest Health Management International; John D. Byrd, Mississippi State University; Howard F. Schwartz, Colorado State University,

Leafy spurge (Euphorbia esula) Kudzu

(Pueraria montana var. lobata)

Understanding plant behavioral responses can contribute to combatting highly competitive invasive species…

And to developing novel crop combinations, such as the intercropping of dry beans, coffee and papaya near Palmira, Colombia


Do invasive plants have shared phenotypes?

Davidson, A.M., Jennions, M. and Nicotra, A.B. (2011). Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecolo.Lett. 14: 419-431. Godoy, O., Valladares, F. and Castro-Díez, P. (2011). Multispecies comparison reveals that invasive and native plants differ in their traits but not in their plasticity. Funct. Ecol. 25: 1248-1259. Jil Swearingen, USDI National Park Service,

C EDBA

Are invasive plants more plastic, and so more able to succeed in diverse environments?

Some invasive plants show greater than average phenotypic plasticity, but many do not.

Some invasive plants succeed by making lots of small seeds, growing very quickly, producing allelochemicals, or competing effectively for water or nutrients

Kudzu (Pueraria lobata), also known as “The vine that ate the South”


Case study: Knotweed, “from prize-winners to pariahs”

See Bailey, J. P., and Conolly, A. P. (2000). Prize-winners to pariahs - a history of Japanese knotweed s.l. (Polygonaceae) in the British Isles. Watsonia 23: 93-110; Murrell, C., Gerber, E., Krebs, C., Parepa, M., Schaffner, U. and Bossdorf, O. (2011). Invasive knotweed affects native plants through allelopathy. Am. J. Bot. 98: 38-43, Richards, C.L., et al., (2008). Plasticity in salt tolerance traits allows for invasion of novel habitat by Japanese knotweed s. l. (Fallopia japonica and F.×bohemica, Polygonaceae). Am. J. Bot. 95: 931-942. Photo credit Fallopia japonica MdE 2.jpg, © MdE at Wikimedia Commons, CC-BY-SA 3.0 German.

Prize-winnersIn 1847, the Society of Agriculture & Horticultureawarded a gold medal to Fallopia japonica, “for the most interesting new ornamental plant of the year”

PariahsNow they are one of the most aggressive plant invaders, and cause considerable economic and ecological damage.

Allelochemical production and rapid growth rate contribute to their ecosystem dominance

Knotweed shows a highly plastic response to salt, which allows it to succeed in salty environments


Case study: Backfiring biocontrol of invasive knapweed?

See Callaway, R.M., DeLuca, T.H. and Belliveau, W.M. (1999). Biological-control of herbivores may increase competitive ability of the noxious weed Centaurea maculosa. Ecology. 80: 1196-1201; Knochel, D.G. and Seastedt, T.R. (2010). Reconciling contradictory findings of herbivore impacts on spotted knapweed ( Centaurea stoebe) growth and reproduction. Ecol. Appl. 20: 1903-1912.Photo credits: L.L. Berry, Bugwood.org; USDA Agricultural Research Service Archive, Bugwood.org; Steve Dewey, Utah State University, Bugwood.org

Spotted knapweed (Centaurea stobe ssp. micranthos / Centaurea maculosa) was introduced into North America in the 1890s. It is a “noxious weed” that competes very effectively with native plants

Agapeta zoegana

Starting in the 1980s, the specific herbivore knapweed root moth has been introduced as a biocontrol agent, with mixed results

Herbivory may induce allelochemical production, further harming native plants – a case of biocontrol backfiring!


Case study: Maize, bean, squash – the three sisters

Photo credit: Howard F. Schwartz, Colorado State University, Bugwood.org; Reprinted from Postma, J.A. and Lynch, J.P. (2012). Complementarity in root architecture for nutrient uptake in ancient maize/bean and maize/bean/squash polycultures. Ann Bot. 110: 521-534 by permission of Oxford University Press.

Archeological records show that Native Americans have grown corn, beans and squash together for millennia

The corn provides a structure for the climbing bean vines, and the ground-covering squash maintains soil moisture and suppress weeds

A recent study found that the root systems of the three plants are complementary, minimizing belowground competition

Maize Bean Squash


Case study: Push-pull planting systems to enhance productivity

Pests are a particular problem in tropical agriculture. An agronomic system called push-pull was developed to protect corn crops from stem borer caterpillars

See Hassanali, A., Herren, H., Khan, Z.R., Pickett, J.A. and Woodcock, C.M. (2008). Integrated pest management: the push–pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Phil. Trans. R. Soc. B 363: 611-621; Pickett, J.A., Hamilton, M.L., Hooper, A.M., Khan, Z.R. and Midega, C.A.O. (2010). Companion Cropping to Manage Parasitic Plants. Annu. Rev. Phytopath. 48: 161-177. Push-pull.net

This involves intercropping maize with a legume Desmodium, in a field surrounded by Napier grass (Pennisetum purpureum)


Case study: Push-pull planting systems to enhance productivity

Reprinted from Khan, Z.R., Midega, C.A.O., Bruce, T.J.A., Hooper, A.M. and Pickett, J.A. (2010). Exploiting phytochemicals for developing a ‘push–pull’ crop protection strategy for cereal farmers in Africa. J. Exp. Bot. 61: 4185-4196, by permission of Oxford University Press.

Desmodium also produces allelochemicals that interfere with Striga parasitism, protecting the crop from yet another pest

Desmodium PUSHES away the insects by producing repellent volatile chemicals

Napier grass PULLS away the insects by producing attractive volatile chemicals


Case study: Allelopathic rice plants

Image source: IRRI. Belz, R.G. (2007). See also Allelopathy in crop/weed interactions — an update. Pest Management Science. 63: 308-326.

Momilactones are allelopathic compounds produced by rice that interfere with the growth of a common paddy weed, barnyard grass (Echinochloa crus-galli)

Momilactone B

Efforts are underway to increase momilactone production in cultivated rice varieties, to reduce the need for herbicide use and mechanical weed removal


Case study: Exploiting light-response plasticity for increased productivity

Greenhouse covers, including a fluorescent pigment that absorbs some of the blue and green sunlight and emits additional red light, increases the ratio between RED and FAR-RED light.

In response to such spectral cues, some plants reduce their allocation to competitive organs and increase allocation to agriculturally-important organs such as flowers and fruits. LEDs can produce similar effects.

Novoplansky, A., T. Sachs, D. Cohen, R. Bar, J. Budenheimer and R. Reisfeld (1990) Increasing plant productivity by changing the solar spectrum. Solar Energy Materials 21: 17-23. See also Stamps, R.H. (2009). Use of colored shade netting in horticulture. HortScience. 44: 239-241. .


Partially adapted from Cahill, J.F. and McNickle, G.G. (2011). The behavioral ecology of nutrient foraging by plants. Annu. Rev. Ecol. Evol. System. 42: 289-311.

Summary of plant-plant interactions

A plant’s phenotype depends on its genotype and environment, and relies on its plasticity. The environment includes cues from and interactions with other plants, many of which we are just beginning to understand, and which continue to be very active research areas

A plant’s phenotype depends on its genotype and environment, and relies on its plasticity. The environment includes cues from and interactions with other plants, many of which we are just beginning to understand, and which continue to be very active research areas

Plasticity

Stochasticity

Fixed development

Phenotype Ecological interactions

Local conditions

Genotype

Cues from other plants

Interactions with other

plants

Biodiversity

Ecosystem functioning

Plant production and

agriculture

Evolution


Reprinted from Kegge, W. and Pierik, R. (2010). Biogenic volatile organic compounds and plant competition. Trends Plant Sci. 15: 126-132 with permission from Elsevier.

Summary of plant-plant interactions

Plants perceive other plants through changes in the light spectrum, volatile and root-exuded chemicals, effects on nutrients, water and soil microbes, and other unknown signals

Their responses depend on their age, genotype and other endogenous and exogenous factors, and may include confrontation, avoidance or tolerance


Future directions (1)

Aggressive aliens, moved by human actions, damage ecosystems

Can fragile ecosystems and biological diversity be protected by better understanding plant – plant interactions?

Can fragile ecosystems and biological diversity be protected by better understanding plant – plant interactions?

Japanese knotweed(Fallopia japonica )

Giant hogweed(Heracleum mantegazzianum)

Photo credits: Fallopia japonica MdE 2.jpg, © MdE at Wikimedia Commons, CC-BY-SA 3.0 German. Randy Westbrooks, U.S. Geological Survey



David Nance USDA ARS Bugwood.org

Can food yields be increased by suppressing competition and competitive responses, enhancing facilitation and increasing production of desired organs?

Can food yields be increased by suppressing competition and competitive responses, enhancing facilitation and increasing production of desired organs?

• Human population growth demands more food production, and higher crop yields

• Plant-plant interactions can decrease yields, but these effects can be ameliorated



Can crop yields be increased, especially in marginal agricultural land, by inducing and priming plants to better fit their particular expected growth conditions, forthcoming opportunities and stresses?

Can crop yields be increased, especially in marginal agricultural land, by inducing and priming plants to better fit their particular expected growth conditions, forthcoming opportunities and stresses?

J.S. Quick, Bugwood.org

Documents

© 2013 American Society of Plant Biologists Plant-plant interactions Photo courtesy of Ronald PierikRonald Pierik