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Competing neighbors: light perception and root function

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Abstract

Plant responses to competition have often been described as passive consequences of reduced resource availability. However, plants have mechanisms to forage for favorable conditions and anticipate competition scenarios. Despite the progresses made in understanding the role of light signaling in modulating plant–plant interactions, little is known about how plants use and integrate information gathered by their photoreceptors aboveground to regulate performance belowground. Given that the phytochrome family of photoreceptors plays a key role in the acquisition of information about the proximity of neighbors and canopy cover, it is tempting to speculate that changes in the red:far-red (R:FR) ratio perceived by aboveground plant parts have important implications shaping plant behavior belowground. Exploring data from published experiments, we assess the neglected role of light signaling in the control of root function. The available evidence indicates that plant exposure to low R:FR ratios affects root growth and morphology, root exudate profiles, and interactions with beneficial soil microorganisms. Although dependent on species identity, signals perceived aboveground are likely to affect root-to-root interactions. Root systems could also be guided to deploy new growth predominantly in open areas by light signals perceived by the shoots. Studying interactions between above- and belowground plant–plant signaling is expected to improve our understanding of the mechanisms of plant competition.

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References

  • Abdel-Lateif K, Bogusz D, Hocher V (2012) The role of flavonoids in the establishment of plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signal Behav 7:636–641

    CAS  PubMed Central  PubMed  Google Scholar 

  • Agrawal AA, Kearney EE, Hastings AP, Ramsey TE (2012) Attenuation of the jasmonate burst, plant defensive traits, and resistance to specialist monarch caterpillars on shaded common milkweed (Asclepias syriaca). J Chem Ecol 38:893–901

    CAS  PubMed  Google Scholar 

  • Akiyama K, Matsuzaki KI, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    CAS  PubMed  Google Scholar 

  • Aphalo PJ, Ballaré CL (1995) On the importance of information-acquiring systems in plant–plant interactions. Funct Ecol 9:5–14

    Google Scholar 

  • Aphalo PJ, Lehto T (2001) Effect of lateral far-red light supplementation on the growth and morphology of birch seedlings and its interaction with mineral nutrition. Trees 15:297–303

    CAS  Google Scholar 

  • Araya T, Miyamoto M, Wibowo J, Suzuki A, Kojima S, Tsuchiya Y, Sawa S, Fukuda H, von Wirén N, Takahashi H (2014) CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proc Natl Acad Sci USA 111:2029–2034

    CAS  PubMed Central  PubMed  Google Scholar 

  • Atkinson D, Naylor D, Coldrick GA (1976) The effect of tree spacing on the apple root system. Hortic Res 16:89–105

    Google Scholar 

  • Bae G, Choi G (2008) Decoding of light signals by plant phytochromes and their interacting proteins. Annu Rev Plant Biol 59:281–311

    CAS  PubMed  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    CAS  PubMed  Google Scholar 

  • Ballare CL (2014) Light and plant defense. Annu Rev Plant Biol 65:335–363

    CAS  PubMed  Google Scholar 

  • Ballaré CL (2009) Illuminated behaviour: phytochrome as a key regulator of light foraging and plant anti-herbivore defence. Plant Cell Environ 32:713–725

    PubMed  Google Scholar 

  • Ballaré CL (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16:249–257

    PubMed  Google Scholar 

  • Ballaré CL, Scopel AL, Sánchez RA (1990) Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies. Science 247:329–332

    PubMed  Google Scholar 

  • Ballaré CL, Scopel AL, Sánchez RA (1991) On the opportunity cost of the photosynthate invested in stem elongation reactions mediated by phytochrome. Oecologia 86:561–567

    Google Scholar 

  • Ballaré CL, Mazza CA, Austin AT, Pierik R (2012) Canopy light and plant health. Plant Physiol 160:145–155

    PubMed Central  PubMed  Google Scholar 

  • Benech-Arnold RL, Sánchez RA, Forcella F, Kruk BC, Ghersa CM (2000) Environmental control of dormancy in weed seed banks in soil. Field Crops Res 67:105–122

    Google Scholar 

  • Biedrzycki ML, Jilany TA, Dudley SA, Bais HP (2010) Root exudates mediate kin recognition in plants. Commun Integr Biol 3:28–35

    PubMed Central  PubMed  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    CAS  PubMed  Google Scholar 

  • Boccalandro HE, De Simone SN, Bergmann-Honsberger A, Schepens I, Fankhauser C, Casal JJ (2008) PHYTOCHROME KINASE SUBSTRATE1 regulates root phototropism and gravitropism. Plant Physiol 146:108–115

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brewer PB, Koltai H, Beveridge CA (2013) Diverse roles of strigolactones in plant development. Mol Plant 6:18–28

    CAS  PubMed  Google Scholar 

  • Briggs WR, Christi JM (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci 7:204–210

    CAS  PubMed  Google Scholar 

  • Brisson J, Reynolds JF (1994) The effect of neighbors on root distribution in a creosotebush (Larrea tridentata) population. Ecology 75:1693–1702

    Google Scholar 

  • Caffaro MM, Vivanco JM, Gutierrez Boem FH, Rubio G (2011) The effect of root exudates on root architecture in Arabidopsis thaliana. Plant Growth Regul 64:241–249

    CAS  Google Scholar 

  • Caffaro MM, Vivanco JM, Botto J, Rubio G (2013) Root architecture of Arabidopsis is affected by competition with neighbouring plants. Plant Growth Regul 70:141–147

    CAS  Google Scholar 

  • Cahill JF Jr, McNickle GG (2011) The behavioral ecology of nutrient foraging by plants. Annu Rev Ecol Evol Syst 42:289–311

    Google Scholar 

  • Cahill JF Jr, McNickle GG, Haag JJ, Lamb EG, Nyanumba SM, Clair St CC (2010) Plants integrate information about nutrients and neighbors. Science 328:1657

    CAS  PubMed  Google Scholar 

  • Carabelli M, Possenti M, Sessa G, Ciolfi A, Sassi M, Morelli G, Ruberti I (2007) Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity. Genes Dev 21:1863–1868

    CAS  PubMed Central  PubMed  Google Scholar 

  • Casal JJ (2013) Photoreceptor signaling networks in plant responses to shade. Annu Rev Plant Biol 64:403–427

    CAS  PubMed  Google Scholar 

  • Cerdán PD, Chory J (2003) Regulation of flowering time by light quality. Nature 423(6942):881–885

    PubMed  Google Scholar 

  • Cerrudo I, Keller MM, Cargnel MD, Demkura PV, de Wit M, Patitucci MS, Pierik R, Pieterse CM, Ballaré CL (2012) Low red/far-red ratios reduce Arabidopsis resistance to Botrytis cinerea and jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism. Plant Physiol 158:2042–2052

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38:87–117

    CAS  PubMed  Google Scholar 

  • Corré WJ (1983) Growth and morphogenesis of sun and shade plants. II. The influence of light quality. Acta Bot Neerl 32:185–202

    Google Scholar 

  • Cowan JE, Reekie EG (2008) Effects of elevated CO2 on intra-specific competition in Sinapis alba: an examination of the role of growth responses to red:far-red ratio. Plant Biol 10:202–210

    CAS  PubMed  Google Scholar 

  • Dale MP, Causton DR (1992) The ecophysiology of Veronica chamaedrys, V. montana and V. officinalis. I. Light quality and light quantity. J Ecol 80:483–492

    Google Scholar 

  • de Kroon H, Mommer L, Nishiwaki A (2003) Root competition: towards a mechanistic understanding. In: de Kroon H, Visser EJW (eds) Root ecology. Springer, Berlin, pp 215–234

    Google Scholar 

  • de la Rosa TM, Aphalo PJ, Lehto T (1998) Effects of far-red light on the growth, mycorrhizas and mineral nutrition of Scots pine seedlings. Plant Soil 201:17–25

    Google Scholar 

  • de la Rosa TM, Lehto T, Aphalo PJ (1999) Does far-red light affect growth and mycorrhizas of Scots pine seedlings grown in forest soil? Plant Soil 211:259–268

    Google Scholar 

  • de Wit M, Kegge W, Evers JB, Vergeer-van Eijk MH, Gankema P, Voesenek LACJ, Pierik R (2012) Plant neighbor detectionn through touching leaf tips precedes phytochrome signals. Proc Natl Acad Sci USA 109:14705–14710

    PubMed Central  PubMed  Google Scholar 

  • de Wit M, Spoel SH, Sánchez-Pérez GF, Gommers CM, Pieterse CM, Voesenek LACJ, Pierik R (2013) Perception of low red:far-red ratio compromises both salicylic acid- and jasmonic acid-dependent pathogen defences in Arabidopsis. Plant J 75:90–103

    PubMed  Google Scholar 

  • Ding ZJ, Galvan-Ampudia CS, Demarsy E, Langowski L, Kleine-Vehn J, Fan YW, Morita MT, Tasaka M, Fankhauser C, Offringa R, Friml J (2011) Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat Cell Biol 13:447–452

    CAS  PubMed  Google Scholar 

  • Dorn LA, Hammond Pyle E, Schmitt J (2000) Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs. Evolution 54:1982–1994

    CAS  PubMed  Google Scholar 

  • Dudley SA, File AL (2007) Kin recognition in an annual plant. Biol Lett 3:435–438

    PubMed Central  PubMed  Google Scholar 

  • Engelen-Eigles G, Holden G, Cohen JD, Gardner G (2006) The effect of temperature, photoperiod and light quality on gluconasturti in concentration in watercress (Nasturtium officinale R. Br.). J Agric Food Chem 54:328–334

    CAS  PubMed  Google Scholar 

  • Falik O, Reides P, Gersani M, Novoplansky A (2003) Self/non-self discrimination in roots. J Ecol 91:525–531

    Google Scholar 

  • Fang S, Clark RT, Zheng Y, Iyer-Pascuzzi AS, Weitz JS, Kochian LV, Edelsbrunner H, Liao H, Benfey PN (2013) Genotypic recognition and spatial responses by rice roots. Proc Natl Acad Sci USA 110:2670–2675

    CAS  PubMed Central  PubMed  Google Scholar 

  • Farley RA, Fitter AH (1999) The responses of seven co-occurring woodland herbaceous perennials to localized nutrient rich patches. J Ecol 87:849–859

    Google Scholar 

  • Feldman LJ, Briggs WR (1987) Light-regulated gravitropism in seedling roots of maize. Plant Physiol 83:241–243

    CAS  PubMed Central  PubMed  Google Scholar 

  • Finlayson SA, Lee I-J, Morgan PW (1998) Phytochrome B and the regulation of circadian ethylene production in Sorghum. Plant Physiol 116:17–25

    CAS  PubMed Central  Google Scholar 

  • Forde BG, Walch-Liu P (2009) Nitrate and glutamate as environmental cues for behavioural responses in plant roots. Plant Cell Environ 32:682–693

    CAS  PubMed  Google Scholar 

  • Frank DA, Pontes AW, Maine EM, Caruana J, Raina R, Raina S, Fridley JD (2010) Grassland root communities: species distributions and how they are linked to aboveground abundance. Ecology 91:3201–3209

    PubMed  Google Scholar 

  • Franklin KA (2008) Shade avoidance. New Phytol 179:930–944

    CAS  PubMed  Google Scholar 

  • Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61:11–24

    CAS  PubMed Central  PubMed  Google Scholar 

  • Franklin KA, Whitelam GC (2004) Light signals, phytochromes and cross-talk with other environmental cues. J Exp Bot 55:271–276

    CAS  PubMed  Google Scholar 

  • Galen C, Rabenold J, Liscum E (2006) Functional ecology of a blue light photoreceptor: effects of phototropin-1 on root growth enhance drought tolerance in Arabidopsis thaliana. New Phytol 173:91–99

    Google Scholar 

  • Gersani M, Abramsky Z, Falik O (1998) Density-dependent habitat selection in plants. Evol Ecol 12:223–234

    Google Scholar 

  • Gersani M, Brown JS, O’Brien EE, Maina GM, Abramsky Z (2001) Tragedy of the commons as a result of root competition. J Ecol 89:660–669

    Google Scholar 

  • Gommers CMM, Visser EJW, Onge St KR, Voesenek LACJ, Pierik R (2013) Shade tolerance: when growing tall is not an option. Trends Plant Sci 18:65–71

    CAS  PubMed  Google Scholar 

  • Green-Tracewicz E, Page ER, Swanton CJ (2012) Light quality and the critical period for weed control in soybean. Weed Sci 60:86–91

    CAS  Google Scholar 

  • Grimes DW, Miller RJ, Wiley PL (1975) Cotton and corn root development in two field soils of different strength characteristics. Agron J 67:519–523

    Google Scholar 

  • Gruntman M, Novoplansky A (2004) Physiologically mediated self non-self discrimination in roots. Proc Natl Acad Sci USA 101:3863–3867

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hendriks M, Mommer L, de Caluwe H, Smit-Tiekstra AE, van der Putten WH, de Kroon H (2013) Independent variations of plant and soil mixtures reveal soil feedback effects on plant community overyielding. J Ecol 101:287–297

    Google Scholar 

  • Hennig L, Stoddart WM, Dieterle M, Whitelam GC, Schäfer E (2002) Phytochrome E controls light-induced germination of Arabidopsis. Plant Physiol 128:194–200

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hess L, de Kroon H (2007) Effects of rooting volume and nutrient availability as an alternative explanation for root self/non-self discrimination. J Ecol 95:241–251

    Google Scholar 

  • Ho C, Tsay Y (2010) Nitrate, ammonium and potassium sensing and signaling. Curr Opin Plant Biol 13:604–610

    CAS  PubMed  Google Scholar 

  • Ho C, Lin S, Hu H, Tsay Y (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194

    CAS  PubMed  Google Scholar 

  • Hoddinott J, Hall LM (1982) The responses of photosynthesis and translocation rates to changes in the ζ ratio of light. Can J Bot 60:1285–1291

    Google Scholar 

  • Hoddinott J, Rickey S (1996) The influence of light quality and carbon dioxide enrichment on the growth and physiology of seedlings of three conifer species. I. Growth responses. Can J Bot 74:383–390

    Google Scholar 

  • Hodge A (2009) Root decisions. Plant Cell Environ 32:628–640

    PubMed  Google Scholar 

  • Holmes MG, Smith H (1977) The function of phytochrome in the natural environment. I. Characterization of daylight for studies in photomorphogesis and photoperiodism. Photochem Photobiol 25:533–538

    Google Scholar 

  • Hornitschek P, Kohnen MV, Lorrain S, Rougemont J, Ljung K, López-Vidriero I, Franco-Zorrilla JM, Solano R, Trevisan M, Pradervand S, Xenarios I, Fankhauser C (2012) Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J 71:699–711

    CAS  PubMed  Google Scholar 

  • Izaguirre MM, Mazza CA, Biondini M, Baldwin IT, Ballaré CL (2006) Remote sensing of future competitors: impacts on plant defenses. Proc Natl Acad Sci 103:7170–7174

    CAS  PubMed Central  PubMed  Google Scholar 

  • Izaguirre MM, Mazza CA, Astigueta MS, Ciarla AM, Ballaré CL (2013) No time for candy: passionfruit (Passiflora edulis) plants down-regulate damage-induced extra floral nectar production in response to light signals of competition. Oecologia 173:213–221

    PubMed  Google Scholar 

  • Jones FA, Erickson DL, Bernal MA, Bermingham E, Kress WJ, Herre EA, Muller-Landau HC, Turner BL (2011) The roots of diversity: below ground species richness and rooting distributions in a tropical forest revealed by DNA barcodes and inverse modeling. PLoS One 6(9):e24506. doi:10.1371/journal.pone.0024506

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kasperbauer MJ, Hunt PG (1992) Cotton seedling morphogenic responses to FR/R ratio reflected from different colored soils and soil covers. Photochem Photobiol 56:579–584

    Google Scholar 

  • Kasperbauer MJ, Hunt PG (1994) Shoot/root assimilate allocation and nodulation of Vigna unguiculata seedlings as influenced by shoot light environment. Plant Soil 161:97–101

    Google Scholar 

  • Kasperbauer MJ, Karlen DL (1994) Plant spacing and reflected far-red light effects on phytochrome-regulated photosynthate allocation in corn seedlings. Crop Sci 34:1564–1569

    CAS  Google Scholar 

  • Kasperbauer MJ, Hunt PG, Sojka RE (1984) Photosynthate partitioning and nodule formation in soybean plants that received red or far-red light at the end of the photosynthetic period. Physiol Plant 61:549–554

    Google Scholar 

  • Kegge W, Pierik R (2010) Biogenic volatile organic compounds and plant competition. Trends Plant Sci 15:126–132

    CAS  PubMed  Google Scholar 

  • Kegge W, Weldegergis B, Soler R, Vegeer-van Eijck M, Dicke M, Voesenek LACJ, Pierik R (2013) Canopy light cues affect emission of constitutive and methyl jasmonate-induced volatile organic compounds in Arabidopsis thaliana. New Phytol 200:861–874

    CAS  PubMed  Google Scholar 

  • Keiller D, Smith H (1989) Control of carbon partitioning by light-quality mediated by phytochrome. Plant Sci 63:25–29

    CAS  Google Scholar 

  • Keller MM, Jaillais Y, Pedmale UV, Moreno JE, Chory J, Ballaré CL (2011) Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially-independent hormonal cascades. Plant J 67:195–207

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kembel SW, Cahill JF Jr (2005) Plant phenotypic plasticity belowground: a phylogenetic perspective on root foraging trade-offs. Am Nat 166:216–230

    PubMed  Google Scholar 

  • Kesanakurti PR, Fazekas AJ, Burgess KS, Percy DM, Newmaster SG, Graham SW, Barrett SC, Hajibabaei M, Husband BC (2011) Spatial patterns of plant diversity below-ground as revealed by DNA barcoding. Mol Ecol 20:1289–1302

    PubMed  Google Scholar 

  • Keuskamp DH, Pollmann S, Voesenek LACJ, Peeters AJM, Pierik R (2010) Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proc Natl Acad Sci USA 107:22740–22744

    CAS  PubMed Central  PubMed  Google Scholar 

  • Keuskamp DH, Sasidharan R, Vos I, Peeters AJM, Voesenek LACJ, Pierik R (2011) Blue-light-mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings. Plant J 67:208–217

    CAS  PubMed  Google Scholar 

  • Klemens JA (2008) Kin recognition in plants? Biol Lett 4:67–68

    PubMed Central  PubMed  Google Scholar 

  • Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K, Zazimalova E, Benkova E, Nacry P, Gojon A (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18:927–937

    CAS  PubMed  Google Scholar 

  • Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv Ecol Res 23:187–261

    CAS  Google Scholar 

  • Lee DW, Baskaran K, Mansor M, Mohamad H, Yap SK (1996) Irradiance and spectral quality affect Asian tropical rain forest tree seedling development. Ecology 77:568–580

    Google Scholar 

  • Li L, Ljung K, Breton G, Schmitz RJ, Pruneda-Paz J, Cowing-Zitron C, Cole BJ, Ivans LJ, Pedmale UV, Jung H-S, Ecker JR, Kay SA, Chory J (2012) Linking photoreceptor excitation to changes in plant architecture. Genes Dev 26:785–790

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu JG, Mahoney KJ, Sikkema PH, Swanton CJ (2009) The importance of light quality in crop–weed competition. Weed Res 49:217–224

    Google Scholar 

  • Lobet G, Pagès L, Draye X (2011) A novel image-analysis toolbox enabling quantitative analysis of root system architecture. Plant Physiol 157:29–39

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lötscher M, Nösberger J (1997) Branch and root formation in Trifolium repens is influenced by the light environment of unfolded leaves. Oecologia 111:499–504

    Google Scholar 

  • Lu YT, Hidaka H, Feldman LJ (1996) Characterization of a calcium/calmodulin-dependent protein kinase homolog from maize roots showing light-regulated gravitropism. Planta 199:18–24

    CAS  PubMed  Google Scholar 

  • Mahall BE, Callaway RM (1991) Root communication among desert shrubs. Proc Natl Acad Sci USA 88:874–876

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mahall BE, Callaway RM (1992) Root communication mechanisms and intracommunity distributions of 2 Mojave desert shrubs. Ecology 73:2145–2151

    Google Scholar 

  • Maina GG, Brown JS, Gersani M (2002) Intra-plant versus inter-plant root competition in beans: avoidance, resource matching or tragedy of the commons. Plant Ecol 160:235–247

    Google Scholar 

  • Martínez-García JF, Galstyan A, Salla-Martret M, Cifuentes-Esquivel N, Gallemí M, Bou-Torrent J (2010) Regulatory components of shade avoidance syndrome. Adv Bot Res 53:65–116

    Google Scholar 

  • Mason WK, Rowse HR, Bennie ATP, Kaspar TC, Taylor HM (1982) Responses of soybeans to two row spacings and two soil water levels. II. Water use, root growth and plant water status. Field Crops Res 5:15–29

    Google Scholar 

  • McKendrick SL (1996) The effects of shade on seedlings of Orchis morio and Dactylorhiza fuchsii in chalk and clay soil. New Phytol 134:343–352

    Google Scholar 

  • McLaren JS, Smith H (1978) Phytochrome control of the growth and development of Rumex obtusifolius under simulated canopy light environments. Plant Cell Environ 1:61–67

    Google Scholar 

  • Mitchell PL, Woodward FI (1988) Responses of three woodland herbs to reduced photosynthetically active radiation and low red to far-red ratio in shade. J Ecol 76:807–825

    Google Scholar 

  • Mommer L, Wagemaker CAM, de Kroon H, Ouborg NJ (2008) Unravelling below-ground plant distributions: a real-time polymerase chain reaction method for quantifying species proportions in mixed root samples. Mol Ecol Resour 8:947–953

    CAS  PubMed  Google Scholar 

  • Mommer L, van Ruijven J, de Caluwe H, Smit-Tiekstra AE, Wagemaker CAM, Joop Ouborg N, Bögemann GM, van der Weerden GM, Berendse F, de Kroon H (2010) Unveiling below-ground species abundance in a biodiversity experiment: a test of vertical niche differentiation among grassland species. J Ecol 98:1117–1127

    Google Scholar 

  • Mommer L, Dumbrell AJ, Wagemaker CAM, Ouborg NJ (2011) Belowground DNA based techniques: untangling the network of plant root interactions. Plant Soil 348:115–121

    CAS  Google Scholar 

  • Mommer L, van Ruijven J, Jansen C, van de Steeg HM, de Kroon H (2012) Interactive effects of nutrient heterogeneity and competition: implications for root foraging theory? Funct Ecol 26:66–73

    Google Scholar 

  • Moreno JE, Tao Y, Chory J, Ballaré CL (2009) Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proc Natl Acad Sci USA 106:4935–4940

    CAS  PubMed Central  PubMed  Google Scholar 

  • Morgan DC, Smith H (1979) A systematic relationship between phytochrome-controlled development and species habitat, for plants grown in simulated natural radiation. Planta 145:253–258

    CAS  PubMed  Google Scholar 

  • Murphy GP, Dudley SA (2007) Above- and below-ground competition cues elicit independent responses. J Ecol 95:261–272

    Google Scholar 

  • Murphy GP, Dudley SA (2009) Kin recognition: competition and cooperation in Impatiens (Balsaminaceae). Am J Bot 96:1990–1996

    PubMed  Google Scholar 

  • Newton AC, Dick JM, McBeath C, Leakey RRB (1996) The influence of R:FR ratio on the growth, photosynthesis and rooting ability of Terminalia spinosa Engl and Triplochiton scleroxylon K. Schum Ann Appl Biol 128:541–556

    Google Scholar 

  • Novoplansky A (2009) Picking battles wisely: plant behaviour under competition. Plant Cell Environ 32:726–741

    PubMed  Google Scholar 

  • O’Brien EE, Gersani M, Brown JS (2005) Root proliferation and seed yield in response to spatial heterogeneity of below-ground competition. New Phytol 168:401–412

    PubMed  Google Scholar 

  • Page ER, Tollenaar M, Lee EA, Lukens L, Swanton CJ (2009) Does the shade avoidance response contribute to the critical period for weed control in maize (Zea mays)? Weed Res 49:563–571

    Google Scholar 

  • Pattison RR, Goldstein G, Ares A (1998) Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. Oecologia 117:449–459

    Google Scholar 

  • Pearson CJ, Jacobs BC (1985) Root distribution in space and time in Trifolium subterranean. Aust J Agric Res 36:601–614

    Google Scholar 

  • Pechácková S (1999) Root response to above-ground light quality. Differences between rhizomatous and non-rhizomatous clones of Festuca rubra. Plant Ecol 141:67–77

    Google Scholar 

  • Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14:399–408

    CAS  PubMed  Google Scholar 

  • Pierik R, Whitelam GC, Voesenek LACJ, de Kroon H, Visser EJW (2004a) Canopy studies on ethylene-insensitive tobacco identify ethylene as a novel element in blue light and plant–plant signaling. Plant J 35:310–319

    Google Scholar 

  • Pierik R, Cuppens MLC, Voesenek LACJ, Visser EJW (2004b) Interactions between ethylene and gibberellins in phytochrome-mediated shade avoidance responses in Tobacco. Plant Physiol 136:2928–2936

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pierik R, Mommer L, Voesenek LACJ (2013) Molecular mechanisms of plant competition: neighbor detection and response strategies. Funct Ecol 27:841–853

    Google Scholar 

  • Pierik R, Ballaré CL, Dicke M (2014) Ecology of plant volatiles: taking a plant community perspective. Plant Cell Environ (in press)

  • Pomilio AD, Leicach SR, Yaber Grass M, Ghersa CM, Santoro M, Vitale A (2000) Root exudate constituents of Avena fatua grown under far infrared enriched light. Phytochem Anal 11:304–308

    CAS  Google Scholar 

  • Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50

    CAS  PubMed  Google Scholar 

  • Rajcan I, Chandler KJ, Swanton CJ (2004) Red-far-red ratio of reflected light: a hypothesis of why early season weed control is important in corn. Weed Sci 52:774–778

    CAS  Google Scholar 

  • Ruberti I, Sessa G, Ciolfi A, Possenti M, Carabelli M, Morelli G (2012) Plant adaptation to dynamically changing environment: the shade avoidance response. Biotechnol Adv 30:1047–1108

    CAS  PubMed  Google Scholar 

  • Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H (2013) The biology of strigolactones. Trends Plant Sci 18:72–83

  • Sadras VO, Hall AJ, Trapani N, Vilella F (1989) Dynamics of rooting and root-length: leaf-area relationships as affected by plant population in sunflower crops. Field Crops Res 22:45–57

    Google Scholar 

  • Salisbury FJ, Hall A, Grierson CS, Halliday KJ (2007) Phytochrome coordinates Arabidopsis shoot and root development. Plant J 50:429–438

    CAS  PubMed  Google Scholar 

  • Schenk HJ (2006) Root competition: beyond resource depletion. J Ecol 94(4):725–739

    Google Scholar 

  • Schmitt J, McCormac AC, Smith H (1995) A test of the adaptive plasticity hypothesis using transgenic and mutant plants disabled in phytochrome-mediated elongation responses to neighbors. Am Nat 146:937–953

    Google Scholar 

  • Semchenko M, John EA, Hutchings MJ (2007) Effects of physical connection and genetic identity of neighbouring ramets on root-placement patterns in two clonal species. New Phytol 176:644–654

    PubMed  Google Scholar 

  • Skálová H, Vosátka M (1998) Growth response of three Festuca rubra clones to light quality and arbuscular mycorrhiza. Folia Geobot 33:159–169

    Google Scholar 

  • Smith H (2000) Phytochromes and light signal perception by plants–an emerging synthesis. Nature 407:585–591

    CAS  PubMed  Google Scholar 

  • Smith H, Whitelam GC (1997) The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Environ 20:840–844

    Google Scholar 

  • Stuefer JF, Huber H (1998) Differential effects of light quantity and spectral light quality on growth, morphology and development in two stoloniferous Potentilla species. Oecologia 117:1–8

    Google Scholar 

  • Suzuki A, Suriyagoda L, Shigeyama T, Tominaga A, Sasaki M, Hiratsuka Y, Yoshinaga A, Arima S, Agarie S, Sakai T, Inada S, Jikumaru Y, Kamiya Y, Uchiumi T, Abe M, Hashiguchi M, Akashi R, Sato S, Kaneko T, Tabata S, Hirsch AM (2011) Lotus japonicus nodulation is photomorphogenetically controlled by sensing the red/far red (R/FR) ratio through jasmonic acid (JA) signaling. Proc Natl Acad Sci USA 108:16837–16842

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tao Y, Ferrer J-L, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, Cheng Y, Lim J, Zhao Y, Ballaré CL, Sandberg G, Noel JP, Chory J (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tegelberg R, Julkunen-Tiitto R, Aphalo PJ (2004) Red:far-red light ratio and UV-B radiation: their effects on leaf phenolics and growth of silver birch seedlings. Plant Cell Environ 27:1005–1013

    CAS  Google Scholar 

  • Tinoco-Ojanguren C, Pearcy RW (1995) A comparison of light quality and quantity effects on the growth and steady-state and dynamic photosynthetic characteristics of three tropical tree species. Funct Ecol 9:222–230

    Google Scholar 

  • Tsuchiya Y, Vidaurre D, Toh S, Hanada A, Nambara E, Kamiya Y, Yamaguchi S, McCourt P (2010) A small–molecule screen identifies new functions for the plant hormone strigolactone. Nat Chem Biol 6:741–749

  • van Hinsberg A (1997) Morphological variation in Plantago lanceolata L.: effects of light quality and growth regulators on sun and shade populations. J Evol Biol 10:687–701

    Google Scholar 

  • van Hinsberg A, van Tienderen P (1997) Variation in growth form in relation to spectral light quality (red/far-red ratio) in Plantago lanceolata L. in sun and shade populations. Oecologia 111:452–459

    Google Scholar 

  • Zavala JA, Mazza CA, Dillon FM, Chludil HD, Ballaré CL (2014) Soybean resistance to stink bugs (Nezara viridula and Piezodorus guildinii) increases with exposure to solar UV-B radiation and correlates with isoflavonoid content in pods under field conditions. Plant Cell Environ (in press)

  • Zhang J, Subramanian S, Stacey G, Yu O (2009) Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. Plant J 57:171–183

    CAS  PubMed  Google Scholar 

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Acknowledgments

This article is dedicated to the memory of Hernán E. Boccalandro with whom P. E. G. started to explore some of the ideas discussed here. P. E. G. thanks Prof. Kari Saikkonen for the opportunity to carry out this project during his post-doctoral stay at MTT Agrifood Research Finland. The stay of P. E. G. at Wageningen University was supported by a visiting scientist grant of the graduate school of Production Ecology and Resource Conservation of Wageningen University and an Academy of Finland grant 137909 (MTT: 21030085).

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Authors and Affiliations

  1. Plant Production Research, MTT Agrifood Research Finland, Jokioinen, Finland

    Pedro E. Gundel

  2. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura, Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad de Buenos Aires, Av. San Martín 4453, C1417DSE, Buenos Aires, Argentina

    Pedro E. Gundel & Carlos L. Ballaré

  3. Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands

    Ronald Pierik

  4. Nature Conservation and Plant Ecology Group, Wageningen University, P.O. Box 47, 6700 AA, Wageningen, The Netherlands

    Liesje Mommer

  5. IIB-INTECH, Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de San Martín, B1650HMP, Buenos Aires, Argentina

    Carlos L. Ballaré

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  1. Pedro E. Gundel
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  2. Ronald Pierik
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  3. Liesje Mommer
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  4. Carlos L. Ballaré
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Correspondence to Pedro E. Gundel.

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Communicated by Fernando Valladares.

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Gundel, P.E., Pierik, R., Mommer, L. et al. Competing neighbors: light perception and root function. Oecologia 176, 1–10 (2014). https://doi.org/10.1007/s00442-014-2983-x

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