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Decrypting Early Perception of Biotic Stress on Plants

  • Simon A. ZebeloEmail author
Living reference work entry
Part of the Reference Series in Phytochemistry book series (RSP)

Abstract

Plant response to biotic stress induced by various herbivores and pathogens involves different defense mechanisms. Plant defense strategies against biotic stressors start in the plasma membrane, where the biotic stressors interact physically by mechanical damage and chemically by introducing elicitors or triggering plant-derived signaling molecules. The concept of “early” is relative and depends on the dynamics of plant cells responding to stimuli. The stimuli triggered by different biotic stressors result in different rates of plant responses, which often depend on the intensity and the rate of the stimulus. In plant responses to stimuli, the term “early” is often used to indicate the first visible or detectable plant response. Plant early biotic stress responses vary based on the type of the stressors. Based on the type of stressors, the rate of early responses is classified as (1) early responses to microbes, (2) early responses to herbivores, and (3) early response to nearby plants. This chapter discusses the variability in early plant responses to stimuli caused by biotic stressors and the importance of understanding the timing of plant responses to changing biotic stimuli.

Keywords

Biotic stimuli Early signaling Signal transduction Molecular patterns 

Abbreviations

AM

Arbuscular mycorrhiza

BAK1

Brassinosteroid-insensitive 1 (BRI1)-associated kinase 1

BIK1

Botrytis-induced kinase 1

BRI1

Brassinosteroid-insensitive 1

CCaMK

Calcium−/calmodulin-dependent protein kinase

CDPK

Ca2+-dependent protein kinases

CERK1

Chitin elicitor receptor kinase 1

CSSP

Common symbiotic signaling pathway

DAMPs

Damage-associated molecular patterns

EF-Tu

Elongation factor-Tu

ETI

Effector-triggered immunity

FACs

Fatty acid amino acid conjugates

FLS2

Flagellin-sensitive 2

GA

Gibberellic acid

GLV

Green leaf volatile

HAMPs

Herbivore-associated molecular patterns

IAA

Indole acetic acid

LCO

Lipochitooligosaccharidic

LRR

Leucine-rich repeat

LysM

Lysine motifs

MAMPs

Microbe-associated molecular patterns

MeSA

Methyl salicylate

MTI

MAMP-triggered immunity

NF

Nodulation (Nod) factors

OS

Oral secretions

PAMPs

Pathogen-associated molecular patterns

PGPR

Plant growth-promoting rhizobacteria

PNG

Peptidoglycan

PRRs

Pattern recognition receptors

PTI

PAMP-triggered immunity

RLKs

Receptor-like kinases

RLPs

Receptor-like proteins

ROS

Reactive oxygen species

Vm

Transmembrane potential

WIPK

Wound-induced protein kinase

References

  1. 1.
    Zebelo SA, Maffei ME (2015) Role of early signalling events in plant-insect interactions. J Exp Bot 66:435–448.  https://doi.org/10.1093/jxb/eru480CrossRefPubMedGoogle Scholar
  2. 2.
    Pel MJC, Pieterse CMJ (2013) Microbial recognition and evasion of host immunity. J Exp Bot 64:1237–1248.  https://doi.org/10.1093/jxb/ers262CrossRefPubMedGoogle Scholar
  3. 3.
    Trda L, Boutrot F, Claverie J, Brule D, Dorey S, Poinssot B (2015) Perception of pathogenic or beneficial bacteria and their evasion of host immunity: pattern recognition receptors in the frontline. Front Plant Sci 6:219.  https://doi.org/10.3389/Fpls.2015.00219CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Newman MA, Sundelin T, Nielsen JT, Erbs G (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci 4:139.  https://doi.org/10.3389/Fpls.2013.00139CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Zipfel C (2014) Plant pattern-recognition receptors. Trends Immunol 35:345–351.  https://doi.org/10.1016/j.it.2014.05.004CrossRefPubMedGoogle Scholar
  6. 6.
    Sakamoto T, Deguchi M, Brustolini OJB, Santos AA, Silva FF, Fontes EPB (2012) The tomato RLK superfamily: phylogeny and functional predictions about the role of the LRRII-RLK subfamily in antiviral defense. BMC Plant Biol 12:229.  https://doi.org/10.1186/1471-2229-12-229CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Liu JY, Chen NN, Grant JN, Cheng ZM, Stewart CN, Hewezi T (2015) Soybean kinome: functional classification and gene expression patterns. J Exp Bot 66:1919–1934.  https://doi.org/10.1093/jxb/eru537CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Liu WD, Liu JL, Triplett L, Leach JE, Wang GL (2014) Novel insights into rice innate immunity against bacterial and fungal pathogens. Annu Rev Phytopathol 52:213–241.  https://doi.org/10.1146/annurev-phyto-102313-045926CrossRefPubMedGoogle Scholar
  9. 9.
    Cui HT, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol 66:487–511.  https://doi.org/10.1146/annurev-arplant-050213-040012CrossRefPubMedGoogle Scholar
  10. 10.
    Bricchi I, Bertea CM, Occhipinti A, Paponov IA, Maffei ME (2012) Dynamics of membrane potential variation and gene expression induced by Spodoptera littoralis, Myzus persicae, and Pseudomonas syringae in Arabidopsis. PLoS One 7(10):e46673.  https://doi.org/10.1371/journal.pone.0046673CrossRefGoogle Scholar
  11. 11.
    Wu SJ, Shan LB, He P (2014) Microbial signature-triggered plant defense responses and early signaling mechanisms. Plant Sci 228:118–126.  https://doi.org/10.1016/j.plantsci.2014.03.001CrossRefPubMedGoogle Scholar
  12. 12.
    Sun YD, Li L, Macho AP, Han ZF, Hu ZH, Zipfel C, Zhou JM, Chai JJ (2013) Structural basis for flg22-induced activation of the arabidopsis FLS2-BAK1 immune complex. Science 342:624–628.  https://doi.org/10.1126/science.1243825CrossRefPubMedGoogle Scholar
  13. 13.
    Schulze B, Mentzel T, Jehle AK, Mueller K, Beeler S, Boller T, Felix G, Chinchilla D (2010) Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem 285:9444–9451.  https://doi.org/10.1074/jbc.M109.096842CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Jeworutzki E, Roelfsema MRG, Anschutz U, Krol E, Elzenga JTM, Felix G, Boller T, Hedrich R, Becker D (2010) Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca2+−associated opening of plasma membrane anion channels. Plant J 62:367–378.  https://doi.org/10.1111/j.1365-313X.2010.04155.xCrossRefPubMedGoogle Scholar
  15. 15.
    Willmann R et al (2011) Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc Natl Acad Sci USA 108:19824–19829.  https://doi.org/10.1073/pnas.1112862108CrossRefPubMedGoogle Scholar
  16. 16.
    Liu B et al (2012) Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24:3406–3419.  https://doi.org/10.1105/tpc.112.102475CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    De Jonge R et al (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–955.  https://doi.org/10.1126/science.1190859CrossRefPubMedGoogle Scholar
  18. 18.
    Cao YR, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP, Joachimiak A, Stacey G (2014) The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife 3.  https://doi.org/10.7554/eLife.03766
  19. 19.
    Akamatsu A et al (2013) An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential early component of chitin-induced rice immunity. Cell Host Microbe 13:465–476.  https://doi.org/10.1016/j.chom.2013.03.007CrossRefPubMedGoogle Scholar
  20. 20.
    Kishi-Kaboshi M et al (2010) A rice fungal MAMP-responsive MAPK cascade regulates metabolic flow to antimicrobial metabolite synthesis. Plant J 63:599–612.  https://doi.org/10.1111/j.1365-313X.2010.04264.xCrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Shimizu T et al (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64:204–214.  https://doi.org/10.1111/j.1365-313X.2010.04324.xCrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Shinya T, Motoyama N, Ikeda A, Wada M, Kamiya K, Hayafune M, Kaku H, Shibuya N (2012) Functional characterization of CEBiP and CERK1 homologs in arabidopsis and rice reveals the presence of different chitin receptor systems in plants. Plant Cell Physiol 53:1696–1706.  https://doi.org/10.1093/pcp/pcs113CrossRefPubMedGoogle Scholar
  23. 23.
    Liu TT et al (2012) Chitin-induced dimerization activates a plant immune receptor. Science 336:1160–1164.  https://doi.org/10.1126/science.1218867CrossRefPubMedGoogle Scholar
  24. 24.
    Wan JR, Tanaka K, Zhang XC, Son GH, Brechenmacher L, Tran HNN, Stacey G (2012) LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in arabidopsis. Plant Physiol 160:396–406.  https://doi.org/10.1104/pp.112.201699CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Shen Y, Liu N, Li C, Wang X, Xu X, Chen W, Xing G, Zheng W (2017) The early response during the interaction of fungal phytopathogen and host plant. Open Biol 7.  https://doi.org/10.1098/rsob.170057CrossRefGoogle Scholar
  26. 26.
    Brueggeman R, Rostoks N, Kudrna D, Kilian A, Han F, Chen J, Druka A, Steffenson B, Kleinhofs A (2002) The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc Natl Acad Sci U S A 99:9328–9333.  https://doi.org/10.1073/pnas.142284999CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Nirmala J, Drader T, Chen X, Steffenson B, Kleinhofs A (2010) Stem rust spores elicit rapid RPG1 phosphorylation. Mol Plant-Microbe Interact 23:1635–1642.  https://doi.org/10.1094/MPMI-06-10-0136CrossRefPubMedGoogle Scholar
  28. 28.
    Nirmala J, Brueggeman R, Maier C, Clay C, Rostoks N, Kannangara CG, von Wettstein D, Steffenson BJ, Kleinhofs A (2006) Subcellular localization and functions of the barley stem rust resistance receptor-like serine/threonine-specific protein kinase Rpg1. Proc Natl Acad Sci U S A 103:7518–7523.  https://doi.org/10.1073/pnas.0602379103CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Mandadi KK, Scholthof KBG (2013) Plant immune responses against viruses: how does a virus cause disease? Plant Cell 25:1489–1505.  https://doi.org/10.1105/tpc.113.111658CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Korner CJ, Klauser D, Niehl A, Dominguez-Ferreras A, Chinchilla D, Boller T, Heinlein M, Hann DR (2013) The immunity regulator BAK1 contributes to resistance against diverse RNA viruses. Mol Plant Microbe Interact 26:1271–1280.  https://doi.org/10.1094/Mpmi-06-13-0179-RCrossRefPubMedGoogle Scholar
  31. 31.
    Incarbone M, Dunoyer P (2013) RNA silencing and its suppression: novel insights from in planta analyses. Trends Plant Sci 18:382–392.  https://doi.org/10.1016/j.tplants.2013.04.001CrossRefPubMedGoogle Scholar
  32. 32.
    Kube M et al (2014) Analysis of the complete genomes of Acholeplasma brassicae, A. palmae and A. laidlawii and their comparison to the obligate parasites from ‘Candidatus Phytoplasma’. J Mol Microb Biotech 24:19–36.  https://doi.org/10.1159/000354322CrossRefGoogle Scholar
  33. 33.
    Win J et al (2012) Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb Symp Quant Biol 77:235–247.  https://doi.org/10.1101/sqb.2012.77.015933CrossRefPubMedGoogle Scholar
  34. 34.
    MacLean AM, Sugio A, Makarova OV, Findlay KC, Grieve VM, Toth R, Nicolaisen M, Hogenhout SA (2011) Phytoplasma effector SAP54 induces indeterminate leaf-like flower development in Arabidopsis plants. Plant Physiol 157:831–841.  https://doi.org/10.1104/pp.111.181586CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Toruno TY, Music MS, Simi S, Nicolaisen M, Hogenhout SA (2010) Phytoplasma PMU1 exists as linear chromosomal and circular extrachromosomal elements and has enhanced expression in insect vectors compared with plant hosts. Mol Microbiol 77:1406–1415.  https://doi.org/10.1111/j.1365-2958.2010.07296.xCrossRefPubMedGoogle Scholar
  36. 36.
    Caillaud MC, Wirthmueller L, Fabro G, Piquerez SJ, Asai S, Ishaque N, Jones JD (2012) Mechanisms of nuclear suppression of host immunity by effectors from the Arabidopsis downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa). Cold Spring Harb Symp Quant Biol 77:285–293.  https://doi.org/10.1101/sqb.2012.77.015115CrossRefPubMedGoogle Scholar
  37. 37.
    Musetti R, Buxa SV, De Marco F, Loschi A, Polizzotto R, Kogel KH, van Bel AJE (2013) Phytoplasma-triggered Ca2+ influx is involved in sieve-tube blockage. Mol Plant-Microbe Interact 26:379–386.  https://doi.org/10.1094/Mpmi-08-12-0207-RCrossRefPubMedGoogle Scholar
  38. 38.
    Pineda A, Soler R, Weldegergis BT, Shimwela MM, Van Loon JJA, Dicke M (2013) Non-pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid-induced plant volatiles via jasmonic acid signalling. Plant Cell Environ 36:393–404.  https://doi.org/10.1111/j.1365-3040.2012.02581.xCrossRefPubMedGoogle Scholar
  39. 39.
    Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact 25:139–150.  https://doi.org/10.1094/Mpmi-06-11-0179CrossRefPubMedGoogle Scholar
  40. 40.
    Planchamp C, Glauser G, Mauch-Mani B (2015) Root inoculation with Pseudomonas putida KT2440 induces transcriptional and metabolic changes and systemic resistance in maize plants. Front Plant Sci 5:719.  https://doi.org/10.3389/Fpls.2014.00719CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Kumar AS, Lakshmanan V, Caplan JL, Powell D, Czymmek KJ, Levia DF, Bais HP (2012) Rhizobacteria Bacillus subtilis restricts foliar pathogen entry through stomata. Plant J 72:694–706.  https://doi.org/10.1111/j.1365-313X.2012.05116.xCrossRefPubMedGoogle Scholar
  42. 42.
    Lopez-Gomez M, Sandal N, Stougaard J, Boller T (2012) Interplay of flg22-induced defence responses and nodulation in Lotus japonicus. J Exp Bot 63:393–401.  https://doi.org/10.1093/jxb/err291CrossRefPubMedGoogle Scholar
  43. 43.
    Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375.  https://doi.org/10.1146/annurev-phyto-082712-102340CrossRefPubMedGoogle Scholar
  44. 44.
    Liang Y, Cao YR, Tanaka K, Thibivilliers S, Wan JR, Choi J, Kang CH, Qiu J, Stacey G (2013) Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 341:1384–1387.  https://doi.org/10.1126/science.1242736CrossRefPubMedGoogle Scholar
  45. 45.
    Fliegmann J et al (2013) Lipo-chitooligosaccharidic symbiotic signals are recognized by LysM receptor-like kinase LYR3 in the Legume Medicago truncatula. ACS Chem Biol 8:1900–1906.  https://doi.org/10.1021/cb400369uCrossRefPubMedGoogle Scholar
  46. 46.
    Bucher M, Hause B, Krajinski F, Kuster H (2014) Through the doors of perception to function in arbuscular mycorrhizal symbioses. New Phytol 204:833–840.  https://doi.org/10.1111/nph.12862CrossRefPubMedGoogle Scholar
  47. 47.
    Czaja LF, Hogekamp C, Lamm P, Maillet F, Martinez EA, Samain E, Denarie J, Kuster H, Hohnjec N (2012) Transcriptional responses toward diffusible signals from symbiotic microbes reveal MtNFP- and MtDMI3-dependent reprogramming of host gene expression by arbuscular mycorrhizal fungal lipochitooligosaccharides. Plant Physiol 159:1671–1685.  https://doi.org/10.1104/pp.112.195990CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Plett JM, Martin FM (2018) Know your enemy, embrace your friend: using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms. Plant J 93:729–746.  https://doi.org/10.1111/tpj.13802CrossRefPubMedGoogle Scholar
  49. 49.
    Chen M, Arato M, Borghi L, Nouri E, Reinhardt D (2018) Beneficial services of arbuscular mycorrhizal fungi – from ecology to application. Front Plant Sci 9:1270.  https://doi.org/10.3389/fpls.2018.01270CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Rey T, Chatterjee A, Buttay M, Toulotte J, Schornack S (2015) Medicago truncatula symbiosis mutants affected in the interaction with a biotrophic root pathogen. New Phytol 206:497–500.  https://doi.org/10.1111/nph.13233CrossRefPubMedGoogle Scholar
  51. 51.
    Xu S, Zhou WW, Pottinger S, Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific among closely related Nicotiana species. BMC Plant Biol 15:2.  https://doi.org/10.1186/S12870-014-0406-0CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Gouhier-Darimont C, Schmiesing A, Bonnet C, Lassueur S, Reymond P (2013) Signalling of Arabidopsis thaliana response to Pieris brassicae eggs shares similarities with PAMP-triggered immunity. J Exp Bot 64:665–674.  https://doi.org/10.1093/jxb/ers362CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Maffei ME, Arimura GI, Mithoefer A (2012) Natural elicitors, effectors and modulators of plant responses. Nat Prod Rep 29:1288–1303CrossRefGoogle Scholar
  54. 54.
    Huffaker A et al (2013) Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense. Proc Natl Acad Sci USA 110:5707–5712.  https://doi.org/10.1073/pnas.1214668110CrossRefPubMedGoogle Scholar
  55. 55.
    Kanchiswamy CN et al (2010) Regulation of Arabidopsis defense responses against Spodoptera littoralis by CPK-mediated calcium signaling. BMC Plant Biol 10:97.  https://doi.org/10.1186/1471-2229-10-97CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Hu L, Ye M, Kuai P, Ye M, Erb M, Lou Y (2018) OsLRR-RLK1, an early responsive leucine-rich repeat receptor-like kinase, initiates rice defense responses against a chewing herbivore. New Phytol 219:1097–1111.  https://doi.org/10.1111/nph.15247CrossRefPubMedGoogle Scholar
  57. 57.
    Cao YR, Aceti DJ, Sabat G, Song JQ, Makino S, Fox BG, Bent AF (2013) Mutations in FLS2 Ser-938 dissect signaling activation in FLS2-mediated arabidopsis immunity. PLoS Pathog 9:e1003313.  https://doi.org/10.1371/journal.ppat.1003313CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Yang DH, Hettenhausen C, Baldwin IT, Wu JQ (2012) Silencing Nicotiana attenuata calcium-dependent protein kinases, CDPK4 and CDPK5, strongly up-regulates wound- and herbivory-induced jasmonic acid accumulations. Plant Physiol 159:1591–1607.  https://doi.org/10.1104/pp.112.199018CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Camoni L, Barbero F, Aducci P, Maffei ME (2018) Spodoptera littoralis oral secretions inhibit the activity of Phaseolus lunatus plasma membrane H+-ATPase. PLoS One 13:e0202142.  https://doi.org/10.1371/journal.pone.0202142CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Yang DH, Hettenhausen C, Baldwin IT, Wu JQ (2011) BAK1 regulates the accumulation of jasmonic acid and the levels of trypsin proteinase inhibitors in Nicotiana attenuata’s responses to herbivory. J Exp Bot 62:641–652.  https://doi.org/10.1093/jxb/erq298CrossRefPubMedGoogle Scholar
  61. 61.
    Monaghan J et al (2014) The calcium-dependent protein kinase CPK28 buffers plant immunity and regulates BIK1 turnover. Cell Host Microbe 16:605–615.  https://doi.org/10.1016/j.chom.2014.10.007CrossRefPubMedGoogle Scholar
  62. 62.
    Kadota Y et al (2014) Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell 54:43–55.  https://doi.org/10.1016/j.molcel.2014.02.021CrossRefPubMedGoogle Scholar
  63. 63.
    Li L et al (2014) The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15:329–338.  https://doi.org/10.1016/j.chom.2014.02.009CrossRefPubMedGoogle Scholar
  64. 64.
    Agliassa C, Maffei ME (2018) Origanum vulgare Terpenoids Induce Oxidative Stress and Reduce the Feeding Activity of Spodoptera littoralis. Int J Mol Sci 19.  https://doi.org/10.3390/ijms19092805CrossRefGoogle Scholar
  65. 65.
    Prince DC, Drurey C, Zipfel C, Hogenhout SA (2014) The leucine-rich repeat receptor-like kinase brassinosteroid insensitive1-associated kinase1 and the cytochrome P450 phytoalexin deficient3 contribute to innate immunity to aphids in arabidopsis. Plant Physiol 164:2207–2219.  https://doi.org/10.1104/pp.114.235598CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Pierik R, Ballare CL, Dicke M (2014) Ecology of plant volatiles: taking a plant community perspective. Plant Cell Environ 37:1845–1853.  https://doi.org/10.1111/pce.12330CrossRefPubMedGoogle Scholar
  67. 67.
    Carriedo LG, Maloof JN, Brady SM (2016) Molecular control of crop shade avoidance. Curr Opin Plant Biol 30:151–158.  https://doi.org/10.1016/j.pbi.2016.03.005CrossRefPubMedGoogle Scholar
  68. 68.
    Warnasooriya SN, Brutnell TP (2014) Enhancing the productivity of grasses under high-density planting by engineering light responses: from model systems to feedstocks. J Exp Bot 65:2825–2834.  https://doi.org/10.1093/jxb/eru221CrossRefPubMedGoogle Scholar
  69. 69.
    Young NF, Ferguson BJ, Antoniadi I, Bennett MH, Beveridge CA, Turnbull CGN (2014) Conditional auxin response and differential cytokinin profiles in shoot branching mutants. Plant Physiol 165:1723–1736CrossRefGoogle Scholar
  70. 70.
    Bou-Torrent J et al (2014) Plant proximity perception dynamically modulates hormone levels and sensitivity in Arabidopsis. J Exp Bot 65:2937–2947.  https://doi.org/10.1093/jxb/eru083CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Heil M (2014) Herbivore- induced plant volatiles: targets, perception and unanswered questions. New Phytol 204:297–306.  https://doi.org/10.1111/nph.12977CrossRefGoogle Scholar
  72. 72.
    Simpraga M, Takabayashi J, Holopainen JK (2016) Language of plants: where is the word? J Integr Plant Biol 58:343–349.  https://doi.org/10.1111/jipb.12447CrossRefPubMedGoogle Scholar
  73. 73.
    Sugimoto K et al (2014) Intake and transformation to a glycoside of (Z)-3-hexenol from infested neighbors reveals a mode of plant odor reception and defense. Proc Natl Acad Sci USA 111:7144–7149CrossRefGoogle Scholar
  74. 74.
    Manohar M et al (2015) Identification of multiple salicylic acid-binding proteins using two high throughput screens. Front Plant Sci 5:777CrossRefGoogle Scholar
  75. 75.
    Kikuta Y, Ueda H, Nakayama K, Katsuda Y, Ozawa R, Takabayashi J, Hatanaka A, Matsuda K (2011) Specific regulation of pyrethrin biosynthesis in Chrysanthemum cinerariaefolium by a blend of volatiles emitted from artificially damaged conspecific plants. Plant Cell Physiol 52:588–596CrossRefGoogle Scholar
  76. 76.
    Zebelo SA, Matsui K, Ozawa R, Maffei ME (2012) Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicum) plant-to-plant communication. Plant Sci 196:93–100CrossRefGoogle Scholar
  77. 77.
    Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184CrossRefGoogle Scholar
  78. 78.
    Hartikainen K et al (2012) Impact of elevated temperature and ozone on the emission of volatile organic compounds and gas exchange of silver birch (Betula pendula Roth). Environ Exper Bot 84:33–43CrossRefGoogle Scholar
  79. 79.
    Pierik R, Mommer L, Voesenek LACJ (2013) Molecular mechanisms of plant competition: neighbour detection and response strategies. Funct Ecol 27:841–853.  https://doi.org/10.1111/1365-2435.12010CrossRefGoogle Scholar
  80. 80.
    Bouwmeester HJ, Roux C, Lopez-Raez JA, Becard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230CrossRefGoogle Scholar
  81. 81.
    Lopez-Raez JA, Pozo MJ, Garcia-Garrido JM (2011) Strigolactones: a cry for help in the rhizosphere. Botany 89:513–522CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Natural SciencesUniversity of Maryland Eastern ShorePrincess AnneUSA

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