Plant-plant interactions Photo courtesy of Ronald Pierik

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

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 © 2013 American Society of Plant Biologists

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 © 2013 American Society of Plant Biologists

Key definitions and concepts Phenotypic plasticity表型可塑性 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 Low phosphate Low light光 High light Low Red: 远红 外的比率 High Red: Farred ratio High phosphate Low phosphate P水平 Polygonum lapathifolium酸膜 Nicotiana tabacum烟 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. © 2013 American Society of Plant Biologists

Phenotypic plasticity in plants 植物的表型可塑性 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 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. © 2013 American Society of Plant Biologists

Signals and cues convey information Signals are generally considered to be an intended information broadcast and can include: hormones, bacterial metabolites, electrical signals, light quality, stress signals Semaphores are signals Odors and light can be cues Cues are considered to be without intent and can include: Nutrient resources, water, light 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. © 2013 American Society of Plant Biologists

Signals and cues affecting plants INFORMATION Internal Signaling Primary metabolites Hormones Electrical pulses Some hormones, such as ethylene and strigolactones, serve as communication vectors both internally and externally External Cueing Signaling Abiotic: Physical and chemical environment atmospheric, edaphic. Biotic: Secretions, exudates, volatiles etc Biotic only External cueing: Can be observed External signaling: Initially, only a hypothesis. Whether it is adaptive for the emitter as well as the receiver must be determined © 2013 American Society of Plant Biologists

Cues inform decisions about when and how to allocate finite resources Signals and cues indicate the “best bet” 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 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. © 2013 American Society of Plant Biologists

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 © 2013 American Society of Plant Biologists

Plant behavior affects morphological and biochemical phenotypes Shaded Full sun One of the most studied plastic responses is shade-induced stem elongation Plants can’t run away – they have different forms of behavior 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 antinutritive 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. © 2013 American Society of Plant Biologists

Plant behavior is affected by many environmental parameters Abiotic factors: Light, moisture, nutrients, etc. Biotic factors: competitors symbionts, pathogens, herbivores, etc. Genome and epigenome 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 © 2013 American Society of Plant Biologists

Case study: Plasticity of leaf morphology in aquatic plants Submerged leaf phenotype Aerial 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. 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 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. © 2013 American Society of Plant Biologists

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 Photo credit: Tom Donald © 2013 American Society of Plant Biologists

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 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: 611621 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. © 2013 American Society of Plant Biologists

With similar needs, competition between plants can be intense “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 © 2013 American Society of Plant Biologists

Light information governs shoot phenotype, but also affects root development and interactions Nutrient and water distribution and various signals and cues govern root phenotype Plants compete with themselves and others Self-shading Shading by non-self Competition and cues from non-self

Light can be a limiting resource in many environments Trees growing in forests can grow more than 100 meters high, shading plants below them, including their own offspring Photos courtesy Ariel Novoplansky © 2013 American Society of Plant Biologists

Responses to shading: confrontation, avoidance, tolerance Confront Avoid Tolerate Elongation response, Increased apical dominance Growing away from competitors Light- or fire-dependent germination Shade tolerant morphology and physiology 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 © 2013 American Society of Plant Biologists

Plants perceive light levels and color (or- light quantity and quality) Light © 2013 American Society of Plant Biologists

Detection of light levels and quality Plants perceive light through photoreceptors that are sensitive to light of various wavelengths Blue light UV receptors Ultraviolet Short wavelength High energy Red / far-red receptors Infrared Long wavelength Low energy © 2013 American Society of Plant Biologists

Phytochrome detects the boundary of photosynthetically active radiance Action spectrum for photosynthesis Photosynthetically active radiance (PAR) Cryptochrome detects blue (450 nm) light Absorption spectra for chlorophyll and accessory pigments Far- Red light – too little energy for photosynthesis Phytochrome detects both photosynthetically active red light (660 nm) and photosynthetically inactive far-red (730 nm) light © 2013 American Society of Plant Biologists

A low ratio of red to far-red light is indicative of vegetative shading Red light is depleted as light passes through the canopy R FR Shaded PAR Green and red light are not absorbed by the photosynthetic pigments – they reflect and pass through leaves Full sun Phytochrome identifies the ratio of Red to Far-red light (R: FR), an indicator of vegetative shading 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. © 2013 American Society of Plant Biologists

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. © 2013 American Society of Plant Biologists

Transduction of light information downstream of photoreceptors 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 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. © 2013 American Society of Plant Biologists

Shade avoidance is a collection of responses to vegetative shading Light Vegetative shading Delayed or suppressed germination Stem and hypocotyl elongation Petiole elongation, leaf hyponasty, narrow leaves Early flowering Reprinted from Casal, J. J. (2012) Shade Avoidance. The Arabidopsis Book 10: e 0157. doi: 10. 1199/tab. 0157 © 2013 American Society of Plant Biologists

R FR Future Shade? Plants elongate less when wearing a collar that filters out far-red light reflected from adjacent leaves Shade Touch is another cue that signals future competition and stimulates elongation 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. © 2013 American Society of Plant Biologists

Case study: Portulaca oleracea, light responses in recumbent plant 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 Reprinted with permission from Novoplansky, A. , Cohen, D. , and Sachs, T. (1990) How Portulaca seedlings avoid their neighbours. Oecologia 82: 490 -493. © 2013 American Society of Plant Biologists

Future shade can be more important than present shade Filters were set up on opposite sides of Portulaca seedlings The other side Little red Little far-red transmitted and reflected more photosynthetic light but much more far-red than red light Green Portulaca grows away from far-red light, even when it means that they are growing towards less light One side (grey) transmitted very little photosynthetic light, equally low in R and FR Grey 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… 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 Adapted from Novoplansky, A. (1991). Developmental responses of portulaca seedlings to conflicting spectral signals. Oecologia 88: 138 -140. © 2013 American Society of Plant Biologists

Some plants have evolved to tolerate shade – life in the dim lane Shade-tolerant species are adapted to low light environments Photos courtesy Tom Donald and Ariel Novoplansky © 2013 American Society of Plant Biologists

Shade tolerance takes many forms Full sun Shade Su n ad e Sh Long-lived shade-tolerant plants invest relatively more resources into defenses against herbivores and pathogens Defenses Adaptations to maximize light interception: Increased leaf area Leaves oriented to intercept light Leaves positioned to minimize overlap High chlorophyll b to a content Growth rate Reduced stemelongation response 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 © 2013 American Society of Plant Biologists

Dark respiration 10 Light compensation point Typically, shade tolerant plants have a lower rate of respiration in the dark, lower light compensation point, and lower light saturation point CO 2 assimilation (μmol/m 2/sec) Energetics of shade tolerance: max. assimilation, min. expenditure Sun plant Shade plant 0 Light saturation point 0 200 400 800 Light intensity (μmol/m 2/sec) © 2013 American Society of Plant Biologists

Light information: Angle, gradients, quality, and time of day 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! 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. © 2013 American Society of Plant Biologists

Germination plasticity: light and other cues for seed germination 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 Photo credits: Forest & Kim Starr, Starr Environmental; Howard F. Schwartz, Colorado State University, Bugwood. org © 2013 American Society of Plant Biologists

Fire (heat and smoke) can promote seed germination Fire stimulates seed release or germination in some plants Banskia spp, before and after fire Some cones and seed pods are fire-serotinous, opening in response to fire Image sources: pfern, Hesperian, © Kurt Stueber, 2003 © 2013 American Society of Plant Biologists

Karrikins are germination-promoting compounds found in smoke 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…. 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. © 2013 American Society of Plant Biologists

Somatic competition: When plants compete with themselves Plants produce many redundant organs that compete with each other Somatic competition can increase plant performance by putting resources into more successful organs 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? 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. © 2013 American Society of Plant Biologists

Branch autonomy may vary according to circumstances L R Growth rate Full sun L R Full shade L There is experimental evidence to support all three types of responses between shoots: independent, competitive and cooperative R Partial shade L R Independent L R Competitive L R Cooperative 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. © 2013 American Society of Plant Biologists

Case study: Two-shoot peas and correlative inhibition Two shoot peas Removing the shoot from a pea seedling causes two shoots to regenerate – a good system to study somatic competition! “Two-shoot pea” 5 -day old pea Shoot removal 5 days Two equal shoots can co-exist, but very often one becomes dominant and the other dies Why does the smaller shoot die? 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. © 2013 American Society of Plant Biologists

Case study: Two-shoot peas and correlative inhibition A. Dark only: 100% survival of dark shoot B. One dark and one light shoot: 20% survival of dark shoot 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…. A. Dark only 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. B. One dark and one light shoot 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. © 2013 American Society of Plant Biologists

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 Photo credit: Tom Donald © 2013 American Society of Plant Biologists

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 © 2013 American Society of Plant Biologists

Competition belowground: Root growth is extremely plastic When soil resources are abundant, plants allocate less biomass to their roots When nutrient distribution is patchy, roots proliferate in the nutrient rich patches 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: 648654, 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. © 2013 American Society of Plant Biologists

Competition belowground: Root growth is extremely plastic Roots respond to other roots Many studies have found that roots have a tendency to grow away from each other 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. © 2013 American Society of Plant Biologists

Belowground competition: Cues, signals and responses Resource limitation Confront (overproliferate) Root-exuded chemicals Avoid (underproliferate) Other Tolerate © 2013 American Society of Plant Biologists

Plants compete for nutrients, which are frequently limiting for growth 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 Fisher, J. B. , Badgley, G. and Blyth, E. (2012). Global nutrient limitation in terrestrial vegetation. Global Biogeochemical Cycles. 26: GB 3007. Credit: NASA JPL/Caltech. © 2013 American Society of Plant Biologists

Most plants enhance nutrient uptake through associations with mycorrhizal fungi or nitrogenfixing 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 plants Nitrogenfixing bacteria Bacteria in nodules produce reduce atmospheric nitrogen Most plants Mycorrhizal fungi Fungus inside plant root Extensive fungal surface area facilitates nutrient and water uptake Photo credits: Gerald Holmes, Valent USA Corporation, Ulrike Mathesius, Bugwood. org, Sara Wright, USDA; Kristine Nichols, USDA © 2013 American Society of Plant Biologists

In some cases, roots avoid contact or proximity to other roots How do roots respond to the roots of another plant? Plexiglass boxes were set up to record root responses… 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 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. © 2013 American Society of Plant Biologists

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 Reprinted from Cahill, J. F. , Mc. Nickle, 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. © 2013 American Society of Plant Biologists

Many plants make allelochemicals that deter competitors Allelopathic chemicals (allelochemicals) interfere with growth of nearby plants Juglone is an allelochemical produced by black walnut (Juglans nigra) 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. © 2013 American Society of Plant Biologists

Allelochemicals can suppress plant growth directly or indirectly 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 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. © 2013 American Society of Plant Biologists

Summary: Plants compete belowground Besides resource competition, the best understood form of belowground competition is the production of toxic or inhibitory allelochemicals The Monterey manzanita (Arctostaphylos montereyensis) suppresses competitors through allelopathy Additional cues likely contribute to belowground interactions © 2011 David Graber © 2013 American Society of Plant Biologists

Plants can respond differently to self, kin and alien Is that me? You seem familiar… Photo credits: Tom Donald © 2013 American Society of Plant Biologists

Do plants respond differently to relatives and unrelated plants? YES- This study showed that roots tend to avoid roots of plants that are not related Same genotype: More overlap Different genotype: Less overlap - avoidance 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. © 2013 American Society of Plant Biologists

Do roots discriminate self from nonself? A B Yes, plants discriminate self from nonself. Plant B, competing with non-self, makes ~50% more root mass than plant A, competing only with self 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 These studies showed more root growth in the presence of “other” than “self”. What cues and signals are involved? 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. © 2013 American Society of Plant Biologists

S/NS may rely on self recognition, rather than on NS discrimination “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? INTACT TWINS ALIEN 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 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. © 2013 American Society of Plant Biologists

Case study: Parasitic plants are extreme competitors Parasitic Striga infestation • Parasitic plants cost approximately 10 billion USD in crop losses annually Heavy Moderate Light • 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 Striga hermonthica Striga asiatica 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. © 2013 American Society of Plant Biologists

Parasitic plants perceive their hosts through chemical cues Cuscuta pentagona (dodder) uses tropisms, touch and volatile cues, to locate its hosts Host root Host-exuded strigolactones and flavonoids promote germination and attachment of Striga and other parasitic plants Striga 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. © 2013 American Society of Plant Biologists

Facilitative behaviors: Plants benefitting from their neighbors Tempering of harsh abiotic environments Stress cues can induce anticipatory responses Enhancing nutrient uptake 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. © 2013 American Society of Plant Biologists

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 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. © 2013 American Society of Plant Biologists

Plants can protect others from harsh abiotic and biotic environments High Andes Buffered substrate and air temperature, enhanced soil moisture and nutrient content Semi-arid plains of Spain Protection from drought Southern France Protection from browsing Semi arid environment, Jordan Protection from browsing and drought 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, . © 2013 American Society of Plant Biologists

Plants can benefit from amelioration of abiotic stresses by their Wind breaking neighbors • • Increased retention of soil moisture • Improved physical characteristics of soil • Increased soil oxygenation in waterlogged environments • Increased nutrients • Decreased evaporation and soil salinity 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 Photo credits: Tom Donald, Joy Viola, Northeastern University, Bugwood. org © 2013 American Society of Plant Biologists

Intercropping and crop rotation confer many benefits 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 Different crown heights can accommodate different light requirements Legumes increase nitrogen content of soil Rotating crops reduces pest populations Ground-hugging plants can suppress weeds Different root distributions can minimize competition for nutrients 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. © 2013 American Society of Plant Biologists

A common mycorrhizal network can facilitate resource sharing Intercropping with sorghum drastically enhanced flax’s growth (+46% increase). Nutrient uptake was facilitated via the common mycorrhizal network (CMN) Flax Mixed Sorghum 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. © 2013 American Society of Plant Biologists

Case study: Community-level effects of phenotypic plasticity How does phenotypic plasticity and facilitation affect other community members? Variation in root architecture affects the plant communities associated with Quercus douglasii; only shallow-rooted trees compete with grasses 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. © 2013 American Society of Plant Biologists

Cues from other plants can prime plants for defense or tolerance Alarm signals are well described in social animals. Stressed plants may emit cues to which other plants respond Be prepared cues 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 © 2013 American Society of Plant Biologists

Perception of and responses to stress and stress cues Induction and priming of defense responses Mechanical damage Herbivore-derived chemicals Pathogens Volatile compounds Volatile emission Root exudates Stomatal closure Other? Drought or UV light Genomic instability © 2013 American Society of Plant Biologists

Volatile compounds from damaged plants can initiate defenses in others The signal(s) travel through air Sagebrush (Artemisia tridentata) Wild tobacco (Nicotiana attenuata) 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 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 © 2013 American Society of Plant Biologists

What are the active compounds and how far do they spread? methacrolein cis-3 -hexenal trans-2 -hexenal Me. JA cineole 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. © 2013 American Society of Plant Biologists

Why do plants emit volatile signals? • 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 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. © 2013 American Society of Plant Biologists

Case study: Plants may also communicate drought stress Oblivious Stressed Drought, high salt 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. © 2013 American Society of Plant Biologists

Testing for root-to-root and relay communication Novoplansky, A. (2012) Learning plant learning. © 2013 American Society of Plant Biologists

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 Before treatment all the plants had the No response in plants that same did not share their rooting stomatal volume width After treatment, stomatal aperture was reduced in plants whose roots were in contact (directly or indirectly) with the stressed plant Falik O, Mordoch Y, Quansah L, Fait A, Novoplansky A (2011) Rumor has it…: Relay communication of stress cues in plants. PLo. S ONE 6(11): e 23625. 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. © 2013 American Society of Plant Biologists

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 Photo credit: Tom Donald © 2013 American Society of Plant Biologists

Putting knowledge to work Understanding plant behavioral responses can contribute to combatting highly competitive invasive species… Leafy spurge (Euphorbia esula) Water hyacinth (Eichhornia crassipes) And to developing novel crop combinations, such as the intercropping of dry beans, coffee and papaya near Palmira, Colombia Kudzu (Pueraria montana var. lobata) Photo credits: Ted Center, USDA; William M. Ciesla, Forest Health Management International; John D. Byrd, Mississippi State University; Howard F. Schwartz, Colorado State University, © 2013 American Society of Plant Biologists

Do invasive plants have shared phenotypes? Some invasive plants show greater than average phenotypic plasticity, but many do not. A B C D E Are invasive plants more plastic, and so more able to succeed in diverse environments? Kudzu (Pueraria lobata), also known as “The vine that ate the South” Some invasive plants succeed by making lots of small seeds, growing very quickly, producing allelochemicals, or competing effectively for water or nutrients 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, © 2013 American Society of Plant Biologists

Case study: Knotweed, “from prizewinners to pariahs” Prize-winners In 1847, the Society of Agriculture & Horticulture awarded a gold medal to Fallopia japonica, “for the most interesting new ornamental plant of the year” Pariahs Now 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 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 Md. E 2. jpg, © Md. E at Wikimedia Commons, CC-BY-SA 3. 0 German. © 2013 American Society of Plant Biologists

Case study: Backfiring biocontrol of invasive knapweed? Spotted knapweed (Centaurea stobe ssp. micranthos / Centaurea maculosa) was introduced into North America in the 1890 s. It is a “noxious weed” that competes very effectively with native plants Starting in the 1980 s, the specific herbivore knapweed root moth has been introduced as a biocontrol agent, Agapeta zoegana with mixed results Herbivory may induce allelochemical production, further harming native plants – a case of biocontrol backfiring! See Callaway, R. M. , De. Luca, 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 © 2013 American Society of Plant Biologists

Case study: Maize, bean, squash – the three sisters 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 Maize Bean Squash A recent study found that the root systems of the three plants are complementary, minimizing belowground competition 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. © 2013 American Society of Plant Biologists

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 Maize This involves intercropping maize with a legume Desmodium, in a field surrounded by Napier grass (Pennisetum purpureum) Desmodium Napier grass 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 © 2013 American Society of Plant Biologists

Case study: Push-pull planting systems to enhance productivity Desmodium PUSHES away the insects by producing repellent volatile chemicals Napier grass PULLS away the insects by producing attractive volatile chemicals Desmodium also produces allelochemicals that interfere with Striga parasitism, protecting the crop from yet another pest 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. © 2013 American Society of Plant Biologists

Case study: Allelopathic rice plants Momilactone B Momilactones are allelopathic compounds produced by rice that interfere with the growth of a common paddy weed, barnyard grass (Echinochloa crus-galli) Efforts are underway to increase momilactone production in cultivated rice varieties, to reduce the need for herbicide use and mechanical weed removal Image source: IRRI. Belz, R. G. (2007). See also Allelopathy in crop/weed interactions — an update. Pest Management Science. 63: 308 -326. © 2013 American Society of Plant Biologists

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. Hort. Science. 44: 239 -241. . © 2013 American Society of Plant Biologists

Summary of plant-plant interactions Local conditions Cues from other plants Interactions with other plants Genotype Plasticity 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 Biodiversity Stochasticity Fixed development Phenotype Ecological interactions Ecosystem functioning Plant production and agriculture Evolution Partially adapted from Cahill, J. F. and Mc. Nickle, G. G. (2011). The behavioral ecology of nutrient foraging by plants. Annu. Rev. Ecol. Evol. System. 42: 289 -311. © 2013 American Society of Plant Biologists

Summary of plant-plant interactions Plants perceive other plants through changes in the light spectrum, volatile and rootexuded 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 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. © 2013 American Society of Plant Biologists

Future directions (1) Can fragile ecosystems and biological diversity be protected by better understanding plant – plant interactions? Japanese knotweed (Fallopia japonica ) Aggressive aliens, moved by human actions, damage ecosystems Giant hogweed (Heracleum mantegazzianum) Photo credits: Fallopia japonica Md. E 2. jpg, © Md. E at Wikimedia Commons, CC-BY-SA 3. 0 German. Randy Westbrooks, U. S. Geological Survey © 2013 American Society of Plant Biologists

Future directions (2) 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 David Nance USDA ARS Bugwood. org © 2013 American Society of Plant Biologists

Future directions (3) 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 © 2013 American Society of Plant Biologists