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Multitude of Long-Distance Signal Molecules Acting Via Phloem

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Biocommunication of Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 14))

Abstract

As sessile organisms, plants use long-range signalling between organs in order to adapt to their environment. The phloem is an important pathway for such long-distance communication. It transports signals that trigger systemic defence responses to wounding, herbivory and infection by plant pathogens. It also plays a pivotal role for developmental transitions, such as floral induction and tuberization, in response to stimuli perceived by the leaves, and physiological adaptation to nutrient deprivation. The signals involved in these processes include hormones, metabolites, proteins and RNAs, transported by mass flow with the phloem translocation stream. Faster signals, such as electropotential waves, can be propagated by the phloem plasma membrane. Most recent studies showed that these signalling pathways can recruit combinations of signal molecules, and that additional steps, such as molecular ‘hopping’ and amplification, may occur within the phloem tissue. This provides a basis to explain how plants cope with multiple environmental stimuli to confer long-lasting effects against stresses and maintain plant growth and development.

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References

  • Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–1056

    Article  PubMed  CAS  Google Scholar 

  • Abelenda JA, Navarro C, Prat S (2011) From the model to the crop: genes controlling tuber formation in potato. Curr Opin Biotechnol 22:287–292

    Article  PubMed  CAS  Google Scholar 

  • Aki T, Shigyo M, Nakano R, Yoneyama T, Yanagisawa S (2008) Nano scale proteomics revealed the presence of regulatory proteins including three FT-like proteins in phloem and xylem saps from rice. Plant Cell Physiol 49:767–790

    Article  PubMed  CAS  Google Scholar 

  • Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001–1013

    Article  PubMed  CAS  Google Scholar 

  • An H, Roussot C, Suárez-López P, Corbesier L, Vincent C, Piñeiro M, Hepworth S, Mouradov A, Justin S, Turnbull C, Coupland G (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131:3615–3626

    Article  PubMed  CAS  Google Scholar 

  • Attaran E, Zeier TE, Griebel T, Zeier J (2009) Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21:954–971

    Article  PubMed  CAS  Google Scholar 

  • Aung K, Lin S-I, Wu C-C, Huang Y-T, C-l Su, Chiou T-J (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011

    Article  PubMed  CAS  Google Scholar 

  • Ayre BG, Turgeon R (2004) Graft transmission of a floral stimulant derived from CONSTANS. Plant Physiol 135:2271–2278

    Article  PubMed  CAS  Google Scholar 

  • Ayre BG, Keller F, Turgeon R (2003) Symplastic continuity between companion cells and the translocation stream: long-distance transport is controlled by retention and retrieval mechanisms in the phloem. Plant Physiol 131:1518–1528

    Article  PubMed  CAS  Google Scholar 

  • Banerjee AK, Chatterjee M, Yu Y, Suh S-G, Miller WA, Hannapel DJ (2006) Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell 18:3443–3457

    Article  PubMed  CAS  Google Scholar 

  • Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    Article  PubMed  CAS  Google Scholar 

  • Bernier G (1988) The control of floral evocation and morphogenesis. Ann Rev Plant Physiol Plant Mol Biol 39:175–219

    Article  Google Scholar 

  • Bernier G. My favourite flowering image: the role of cytokinin as a flowering signal. J Exp Bot, in press

    Google Scholar 

  • Birkett MA, Campbell CAM, Chamberlain K, Guerrieri E, Hick AJ, Martin JL, Matthes M, Napier JA, Pettersson J, Pickett JA, Poppy GM, Pow EM, Pye BJ, Smart LE, Wadhams GH, Wadhams LJ, Woodcock CM (2000) New roles for cis-jasmone as an insect semiochemical and in plant defense. Proc Natl Acad Sci USA 97:9329–9334

    Article  PubMed  CAS  Google Scholar 

  • Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043

    Article  PubMed  CAS  Google Scholar 

  • Bou-Torrent J, Roig-Villanova I, Martínez-García JF (2008) Light signaling: back to space. Trends Plant Sci 13:108–114

    Article  PubMed  CAS  Google Scholar 

  • Bruce TJA, Pickett JA (2007) Plant defence signalling induced by biotic attacks. Curr Opin Plant Biol 10:387–392

    Article  PubMed  CAS  Google Scholar 

  • Bruce TJA, Matthes MC, Chamberlain K, Woodcock CM, Mohib A, Webster B, Smart LE, Birkett MA, Pickett JA, Napier JA (2008) cis-jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids. Proc Natl Acad Sci USA 105:4553–4558

    Article  PubMed  CAS  Google Scholar 

  • Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J (2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53:739–749

    Article  PubMed  CAS  Google Scholar 

  • Buhtz A, Pieritz J, Springer F, Kehr J (2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64

    Article  PubMed  CAS  Google Scholar 

  • Burleigh SH, Harrison MJ (1999) The down-regulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiol 119:241–248

    Article  PubMed  CAS  Google Scholar 

  • Callos JD, Medford JI (1994) Organ positions and pattern formation in the shoot apex. Plant J 6:1–7

    Article  Google Scholar 

  • Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet-Mercey S, Taconnat L, Renou J-P, Daniel-Vedele F, Fernandez E, Meyer C, Krapp A (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–435

    Article  PubMed  CAS  Google Scholar 

  • Castaings L, Marchive C, Meyer C, Krapp A (2011) Nitrogen signalling in Arabidopsis: how to obtain insights into a complex signalling network. J Exp Bot 62:1391–1397

    Article  PubMed  CAS  Google Scholar 

  • Chailakhyan MK (1936) New facts in support of the hormonal theory of plant development. Dokl Biol Sci 13:79–83

    Google Scholar 

  • Chaturvedi R, Krothapalli K, Makandar R, Nandi A, Sparks AA, Roth MR, Welti R, Shah J (2008) Plastid ω3-fatty acid desaturase-dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant J 54:106–117

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Rosin FM, Prat S, Hannapel DJ (2003) Interacting transcription factors from the three-amino acid loop extension superclass regulate tuber formation. Plant Physiol 132:1391–1404

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Agnew JL, Cohen JD, He P, Shan L, Sheen J, Kunkel BN (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc Natl Acad Sci USA 104:20131–20136

    Article  PubMed  CAS  Google Scholar 

  • Chincinska IA, Liesche J, Krügel U, Michalska J, Geigenberger P, Grimm B, Kühn C (2008) Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol 146:515–528

    Article  PubMed  CAS  Google Scholar 

  • Chiou T-J, Lin S-I (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206

    Article  PubMed  CAS  Google Scholar 

  • Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412–421

    Article  PubMed  CAS  Google Scholar 

  • Conti L, Bradley D (2007) TERMINAL FLOWER1 is a mobile signal controlling Arabidopsis architecture. Plant Cell 19:767–778

    Article  PubMed  CAS  Google Scholar 

  • Cooper HD, Clarkson DT (1989) Cycling of amino-nitrogen and other nutrients between shoots and roots in cereals—a possible mechanism integrating shoot and root in the regulation of nutrient uptake. J Exp Bot 40:753–762

    Article  CAS  Google Scholar 

  • Corbesier L, Coupland G (2005) Photoperiodic flowering of Arabidopsis: integrating genetic and physiological approaches to characterization of the floral stimulus. Plant Cell Environ 28:54–66

    Article  CAS  Google Scholar 

  • Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033

    Article  PubMed  CAS  Google Scholar 

  • Crawford NM, Guo F-Q (2005) New insights into nitric oxide metabolism and regulatory functions. Trends Plant Sci 10:195–200

    Article  PubMed  CAS  Google Scholar 

  • Cui J, Bahrami AK, Pringle EG, Hernandez-Guzman G, Bender CL, Pierce NE, Ausubel FM (2005) Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc Natl Acad Sci USA 102:1791–1796

    Article  PubMed  CAS  Google Scholar 

  • D’Aloia M, Bonhomme D, Bouché F, Tamseddak K, Ormenese S, Torti S, Coupland G, Périlleux C (2011) Cytokinin promotes flowering of Arabidopsis via transcriptional activation of the FT paralogue TSF. Plant J 65:972–979

    Article  PubMed  CAS  Google Scholar 

  • Davis SJ (2009) Integrating hormones into the floral-transition pathway of Arabidopsis thaliana. Plant Cell Environ 32:1201–1210

    Article  PubMed  CAS  Google Scholar 

  • De Torres ZM, Bennett MH, Truman WH, Grant MR (2009) Antagonism between salicylic and abscisic acid reflects early host–pathogen conflict and moulds plant defence responses. Plant J 59:375–386

    Article  CAS  Google Scholar 

  • Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107:207–213

    PubMed  CAS  Google Scholar 

  • Dinant S, Lemoine R (2010) The phloem pathway: new issues and old debates. C R Biol 333:307–319

    Article  PubMed  CAS  Google Scholar 

  • Dinant S, Bonnemain J, Girousse C, Kehr J (2010) Phloem sap intricacy and interplay with aphid feeding. C R Biol 333:504–515

    Article  PubMed  Google Scholar 

  • Ding X, Cao Y, Huang L, Zhao J, Xu C, Li X, Wang S (2008) Activation of the indole-3-acetic acid–amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell 20:228–240

    Article  PubMed  CAS  Google Scholar 

  • Divol F, Vilaine F, Thibivilliers S, Amselem J, Palauqui JC, Kusiak C, Dinant S (2005) Systemic response to aphid infestation by myzus persicae in the phloem of Apium graveolens. Plant Mol Biol 57:517–540

    Article  PubMed  CAS  Google Scholar 

  • Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12:211–221

    Article  PubMed  CAS  Google Scholar 

  • Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374

    Article  PubMed  CAS  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    Article  PubMed  CAS  Google Scholar 

  • Eriksson S, Böhlenius H, Moritz T, Nilsson O (2006) GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation. Plant Cell 18:2172–2181

    Article  PubMed  CAS  Google Scholar 

  • Fan J, Hill L, Crooks C, Doerner P, Lamb C (2009a) Abscisic acid has a key role in modulating diverse plant–pathogen interactions. Plant Physiol 150:1750–1761

    Article  PubMed  CAS  Google Scholar 

  • Fan S-C, Lin C-S, Hsu P-K, Lin S-H, Tsay Y-F (2009b) The Arabidopsis nitrate transporter NRT1.7, expressed in phloem, is responsible for source-to-sink remobilization of nitrate. Plant Cell 21:2750–2761

    Article  PubMed  CAS  Google Scholar 

  • Farmer EE (2001) Surface-to-air signals. Nature 411:854–856

    Article  PubMed  CAS  Google Scholar 

  • Filleur S, Dorbe M-F, Cerezo M, Orsel M, Granier F, Gojon A, Daniel-Vedele F (2001) An Arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake. FEBS Lett 489:220–224

    Article  PubMed  CAS  Google Scholar 

  • Forde BG (2002a) Local and long-range signaling pathways regulating plant responses to nitrate. Annu Rev Plant Biol 53:203–224

    Article  PubMed  CAS  Google Scholar 

  • Forde BG (2002b) The role of long‐distance signalling in plant responses to nitrate and other nutrients. J Exp Bot 53:39–43

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Forouhar F, Yang Y, Kumar D, Chen Y, Fridman E, Park SW, Chiang Y, Acton TB, Montelione GT, Pichersky E, Klessig DF, Tong L (2005) Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc Natl Acad Sci USA 102:1773–1778

    Article  PubMed  CAS  Google Scholar 

  • Franco-Zorrilla JM, Martin AC, Leyva A, Paz-Ares J (2005) Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol 138:847–857

    Article  PubMed  CAS  Google Scholar 

  • Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257

    Article  PubMed  CAS  Google Scholar 

  • Frost CJ, Appel HM, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10:490–498

    Article  PubMed  Google Scholar 

  • Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043

    Article  PubMed  CAS  Google Scholar 

  • Furch AC, Hafke JB, Schulz A, van Bel AJ (2007) Ca2+-Mediated remote control of reversible sieve tube occlusion in Vicia faba. J Exp Bot 58:2827–2838

    Article  PubMed  CAS  Google Scholar 

  • Furch AC, van Bel AJ, Fricker MD, Felle HH, Fuchs M, Hafke JB (2009) Sieve element Ca2+ channels as relay stations between remote stimuli and sieve tube occlusion in Vicia faba. Plant Cell 21:2118–2132

    Article  PubMed  CAS  Google Scholar 

  • Furch ACU, Zimmermann MR, Will T, Hafke JB, van Bel AJE (2010) Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima. J Exp Bot 61:3697–3708

    Article  PubMed  CAS  Google Scholar 

  • Gaupels F, Furch AC, Will T, Mur LA, Kogel KH, van Bel AJ (2008) Nitric oxide generation in Vicia faba phloem cells reveals them to be sensitive detectors as well as possible systemic transducers of stress signals. New Phytol 178:634–646

    Article  PubMed  CAS  Google Scholar 

  • Giakountis A, Coupland G (2008) Phloem transport of flowering signals. Curr Opin Plant Biol 11:687–694

    Article  PubMed  CAS  Google Scholar 

  • Giavalisco P, Kapitza K, Kolasa A, Buhtz A, Kehr J (2006) Towards the proteome of Brassica napus phloem sap. Proteomics 6:896–909

    Article  PubMed  CAS  Google Scholar 

  • Giehl RFH, Meda AR, von Wirén N (2009) Moving up, down, and everywhere: signaling of micronutrients in plants. Curr Opin Plant Biol 12:320–327

    Article  PubMed  CAS  Google Scholar 

  • Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci USA 105:803–808

    Article  PubMed  CAS  Google Scholar 

  • Giordanengo P, Brunissen L, Rusterucci C, Vincent C, van Bel A, Dinant S, Girousse C, Faucher M, Bonnemain JL (2010) Compatible plant-aphid interactions: how aphids manipulate plant responses. C R Biol 333:516–523

    Article  PubMed  Google Scholar 

  • Girin T, El-Kafafi E-S, Widiez T, Erban A, Hubberten H-M, Kopka J, Hoefgen R, Gojon A, Lepetit M (2010) Identification of Arabidopsis mutants impaired in the systemic regulation of root nitrate uptake by the nitrogen status of the plant. Plant Physiol 153:1250–1260

    Article  PubMed  CAS  Google Scholar 

  • Grant M, Lamb C (2006) Systemic immunity. Curr Opin Plant Biol 9:414–420

    Article  PubMed  CAS  Google Scholar 

  • Griebel T, Zeier J (2008) Light regulation and daytime dependency of inducible plant defenses in Arabidopsis: phytochrome signaling controls systemic acquired resistance rather than local defense. Plant Physiol 147:790–801

    Article  PubMed  CAS  Google Scholar 

  • Guo FQ, Wang R, Crawford NM (2002) The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is regulated by auxin in both shoots and roots. J Exp Bot 53:835–844

    Article  PubMed  CAS  Google Scholar 

  • Gutiérrez RA, Stokes TL, Thum K, Xu X, Obertello M, Katari MS, Tanurdzic M, Dean A, Nero DC, McClung CR, Coruzzi GM (2008) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc Natl Acad Sci USA 105:4939–4944

    Article  PubMed  Google Scholar 

  • Hafke JB, van Amerongen JK, Kelling F, Furch AC, Gaupels F, van Bel AJ (2005) Thermodynamic battle for photosynthate acquisition between sieve tubes and adjoining parenchyma in transport phloem. Plant Physiol 138:1527–1537

    Article  PubMed  CAS  Google Scholar 

  • Ham BK, Brandom JL, Xoconostle-Cazares B, Ringgold V, Lough TJ, Lucas WJ (2009) A polypyrimidine tract binding protein, pumpkin RBP50, forms the basis of a phloem-mobile ribonucleoprotein complex. Plant Cell 21:197–215

    Article  PubMed  CAS  Google Scholar 

  • Hause B, Stenzel I, Miersch O, Maucher H, Kramell R, Ziegler J, Wasternack C (2000) Tissue-specific oxylipin signature of tomato flowers: allene oxide cyclase is highly expressed in distinct flower organs and vascular bundles. Plant J 24:113–126

    Article  PubMed  CAS  Google Scholar 

  • Hause B, Hause G, Kutter C, Miersch O, Wasternack C (2003) Enzymes of jasmonate biosynthesis occur in tomato sieve elements. Plant Cell Physiol 44:643–648

    Article  PubMed  CAS  Google Scholar 

  • Hecht V, Laurie RE, Vander Schoor JK, Ridge S, Knowles CL, Liew LC, Sussmilch FC, Murfet IC, Macknight RC, Weller JL (2011) The pea GIGAS gene is a FLOWERING LOCUS T homolog necessary for graft-transmissible specification of flowering but not for responsiveness to photoperiod. Plant Cell 23:147–161

    Article  PubMed  CAS  Google Scholar 

  • Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472

    Article  PubMed  CAS  Google Scholar 

  • Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272

    Article  PubMed  CAS  Google Scholar 

  • Hind SR, Malinowski R, Yalamanchili R, Stratmann JW (2010) Tissue-type specific systemin perception and the elusive systemin receptor. Plant Signal Behav 5:42–44

    Article  PubMed  CAS  Google Scholar 

  • Hoad GV (1995) Transport of hormones in the phloem of higher plants. Plant Growth Regul 16:173–182

    Article  CAS  Google Scholar 

  • Hu H-C, Wang Y-Y, Tsay Y-F (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264–278

    Article  PubMed  CAS  Google Scholar 

  • Ivashikina N, Deeken R, Ache P, Kranz E, Pommerrenig B, Sauer N, Hedrich R (2003) Isolation of AtSUC2 promoter-GFP-marked companion cells for patch-clamp studies and expression profiling. Plant J 36:931–945

    Article  PubMed  CAS  Google Scholar 

  • Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, Shimamoto K (2002) Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes Dev 16:2006–2020

    Article  PubMed  CAS  Google Scholar 

  • Jackson SD, Heyer A, Dietze J, Prat S (1996) Phytochrome B mediates the photoperiodic control of tuber formation in potato. Plant J 9:159–166

    Article  CAS  Google Scholar 

  • Jackson SD, James P, Prat S, Thomas B (1998) Phytochrome B affects the levels of a graft-transmissible signal involved in tuberization. Plant Physiol 117:29–32

    Article  PubMed  CAS  Google Scholar 

  • Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17:1050–1054

    Article  PubMed  CAS  Google Scholar 

  • Jaillais Y, Chory J (2011) Unraveling the paradoxes of plant hormone signaling integration. Nat Struct Mol Biol 17:642–645

    Article  CAS  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324:89–91

    Article  PubMed  CAS  Google Scholar 

  • Kachroo P, Shanklin J, Shah J, Whittle EJ, Klessig DF (2001) A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc Natl Acad Sci USA 98:9448–9453

    Article  PubMed  CAS  Google Scholar 

  • Kachroo A, Venugopal SC, Lapchyk L, Falcone D, Hildebrand D, Kachroo P (2004) Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proc Natl Acad Sci USA 101:5152–5157

    Article  PubMed  CAS  Google Scholar 

  • Kazan K, Manners JM (2008) Jasmonate signaling: toward an integrated view. Plant Physiol 146:1459–1468

    Article  PubMed  CAS  Google Scholar 

  • Kehr J (2009) Long-distance transport of macromolecules through the phloem. F1000. Biol Rep 1:131

    Google Scholar 

  • Kempers R, van Bel AJE (1997) Symplasmic connections between sieve element and companion cell in the stem phloem of Vicia faba L. have a molecular exclusion limit of at least 10 kDa. Planta 201:195–201

    Article  CAS  Google Scholar 

  • Kiefer IW, Slusarenko AJ (2003) The pattern of systemic acquired resistance induction within the Arabidopsis rosette in relation to the pattern of translocation. Plant Physiol 132:840–847

    Article  PubMed  CAS  Google Scholar 

  • Kim M, Canio W, Kessler S, Sinha N (2001) Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293:287–289

    Article  PubMed  CAS  Google Scholar 

  • King RW, Evans LT (2003) Gibberellins and flowering of grasses and cereals: prizing open the lid of the “florigen” black box. Annu Rev Plant Biol 54:307–328

    Article  PubMed  CAS  Google Scholar 

  • King RW, Moritz T, Evans LT, Junttila O, Herlt AJ (2001) Long-day induction of flowering in Lolium temulentum involves sequential increases in specific gibberellins at the shoot apex. Plant Physiol 127:624–632

    Article  PubMed  CAS  Google Scholar 

  • King RW, Moritz T, Evans LT, Martin J, Andersen CH, Blundell C, Kardailsky I, Chandler PM (2006) Regulation of flowering in the long-day grass Lolium temulentum by gibberellins and the FLOWERING LOCUS T gene. Plant Physiol 141:498–507

    Article  PubMed  CAS  Google Scholar 

  • King RW, Mander LN, Asp T, MacMillan CP, Blundell CA, Evans LT (2008) Selective deactivation of gibberellins below the shoot apex is critical to flowering but not to stem elongation of Lolium. Mol Plant 1:295–307

    Article  PubMed  CAS  Google Scholar 

  • Knoblauch M, Peters WS (2010) Münch, morphology, microfluidics—our structural problem with the phloem. Plant Cell Environ 33:1439–1452

    PubMed  Google Scholar 

  • Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962

    Article  PubMed  CAS  Google Scholar 

  • Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol 155:974–987

    Article  PubMed  CAS  Google Scholar 

  • Komiya R, Yokoi S, Shimamoto K (2009) A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136:3443–3450

    Article  PubMed  CAS  Google Scholar 

  • Koo AJK, Howe GA (2009) The wound hormone jasmonate. Phytochemistry 70:1571–1580

    Article  PubMed  CAS  Google Scholar 

  • Koo AJK, Gao X, Daniel Jones A, Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J 59:974–986

    Article  PubMed  CAS  Google Scholar 

  • Krouk G, Crawford NM, Coruzzi GM, Tsay Y-F (2010a) Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Biol 13:265–272

    Article  CAS  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 (2010b) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18:927–937

    Article  PubMed  CAS  Google Scholar 

  • Krouk G, Ruffel S, Gutiérrez RA, Gojon A, Crawford NM, Coruzzi GM, Lacombe B (2011) A framework integrating plant growth with hormones and nutrients. Trends Plant Sci 16:178–182

    Article  PubMed  CAS  Google Scholar 

  • Kumar D, Klessig DF (2003) High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proc Natl Acad Sci USA 100:16101–16106

    Article  PubMed  CAS  Google Scholar 

  • Lalonde S, Tegeder M, Throne-Holst M, Frommer WB, Patrick JW (2003) Phloem loading and unloading of sugars and amino acids. Plant Cell Environ 26:37–56

    Article  CAS  Google Scholar 

  • Lang A (1952) Physiology of flowering. Ann Rev Plant Physiol 3:265–306

    Article  Google Scholar 

  • Laubinger S, Marchal V, Le Gourrierec J, Wenkel S, Adrian J, Jang S, Kulajta C, Braun H, Coupland G, Hoecker U (2006) Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability. Development 133:3213–3222

    Article  PubMed  CAS  Google Scholar 

  • Le Hir R, Beneteau J, Bellini C, Vilaine F, Dinant S (2008) Gene expression profiling: keys for investigating phloem functions. Trends Plant Sci 13:273–280

    Article  PubMed  CAS  Google Scholar 

  • Lee GI, Howe GA (2003) The tomato mutant spr1 is defective in systemin perception and the production of a systemic wound signal for defense gene expression. Plant J 33:567–576

    Article  PubMed  CAS  Google Scholar 

  • Lehesranta SJ, Lichtenberger R, Helariutta Y (2010) Cell-to-cell communication in vascular morphogenesis. Curr Opin Plant Biol 13:59–65

    Article  PubMed  CAS  Google Scholar 

  • Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze: nitric oxide signalling in plant defence. Curr Opin Plant Biol 12:451–458

    Article  PubMed  CAS  Google Scholar 

  • Lejay L, Tillard P, Lepetit M, Olive Francesc D, Filleur S, Daniel-Vedele F, Gojon A (1999) Molecular and functional regulation of two NO3– uptake systems by N- and C-status of Arabidopsis plants. Plant J 18:509–519

    Article  PubMed  CAS  Google Scholar 

  • Lejay L, Gansel X, Cerezo M, Tillard P, Müller C, Krapp A, von Wirén N, Daniel-Vedele F, Gojon A (2003) Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell 15:2218–2232

    Article  PubMed  CAS  Google Scholar 

  • Lejay L, Wirth J, Pervent M, Cross JM-F, Tillard P, Gojon A (2008) Oxidative pentose phosphate pathway-dependent sugar sensing as a mechanism for regulation of root ion transporters by photosynthesis. Plant Physiol 146:2036–2053

    Article  PubMed  CAS  Google Scholar 

  • Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M, Tsuda S, Millenaar FF, Welschen RAM, Ritsema T, Pieterse CMJ (2009) Ethylene modulates the role of nonexpressor of pathogenesis-related genes1 in cross talk between salicylate and jasmonate signaling. Plant Physiol 149:1797–1809

    Article  PubMed  CAS  Google Scholar 

  • Leon-Reyes A, Du Y, Koornneef A, Proietti S, Körbes AP, Memelink J, Pieterse CMJ, Ritsema T (2010) Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Mol Plant Microbe Interact 23:187–197

    Article  PubMed  CAS  Google Scholar 

  • Li C, Dubcovsky J (2008) Wheat FT protein regulates VRN1 transcription through interactions with FDL2. Plant J 55:543–554

    Article  PubMed  CAS  Google Scholar 

  • Li C, Liu G, Xu C, Lee GI, Bauer P, Ling HQ, Ganal MW, Howe GA (2003) The tomato suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell 15:1646–1661

    Article  PubMed  CAS  Google Scholar 

  • Li P, Ham B-K, Lucas WJ (2011) CmRBP50 Protein phosphorylation is essential for assembly of a stable phloem-mobile high-affinity ribonucleoprotein complex. J Biol Chem 286:23142–23149

    Article  PubMed  CAS  Google Scholar 

  • Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci USA 103:6398–6403

    Article  PubMed  CAS  Google Scholar 

  • Lin M-K, Belanger H, Lee YJ, Varkonyi-Gasic E, Taoka K-I, Miura E, Xoconostle-Cázares B, Gendler K, Jorgensen RA, Phinney B, Lough TJ, Lucas WJ (2007) FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell 19:1488–1506

    Article  PubMed  CAS  Google Scholar 

  • Lin S-I, Chiang S-F, Lin W-Y, Chen J-W, Tseng C-Y, Wu P-C, Chiou T-J (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746

    Article  PubMed  CAS  Google Scholar 

  • Linkohr BI, Williamson LC, Fitter AH, Leyser HM (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29:751–760

    Article  PubMed  CAS  Google Scholar 

  • Little DY, Rao H, Oliva S, Fo D-V, Krapp A, Malamy JE (2005) The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. Proc Natl Acad Sci USA 102:13693–13698

    Article  PubMed  CAS  Google Scholar 

  • Liu C, Muchhal US, Uthappa M, Kononowicz AK, Raghothama KG (1998) Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol 116:91–99

    Article  PubMed  CAS  Google Scholar 

  • Liu T-Y, Chang C-Y, Chiou T-J (2009) The long-distance signaling of mineral macronutrients. Curr Opin Plant Biol 12:312–319

    Article  PubMed  CAS  Google Scholar 

  • Liu P-P, von Dahl CC, Park S-W, Klessig DF (2011a) Interconnection between methyl salicylate and lipid-based long-distance signaling during the development of systemic acquired resistance in Arabidopsis and tobacco. Plant Physiol 155:1762–1768

    Article  PubMed  CAS  Google Scholar 

  • Liu T-Y, Aung K, Tseng C-Y, Chang T-Y, Chen Y-S, Chiou T-J (2011b) Vacuolar Ca2+/H+ transport activity is required for systemic phosphate homeostasis involving shoot-to-root signaling in Arabidopsis. Plant Physiol 156:1176–1189

    Google Scholar 

  • López-Ráez JA, Charnikhova T, Gómez-Roldán V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Bécard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874

    Article  PubMed  CAS  Google Scholar 

  • Lough TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Ann Rev Plant Biol 57:203–232

    Article  CAS  Google Scholar 

  • Ma Y, Miura E, Ham B-K, Cheng H-W, Lee Y-J, Lucas WJ (2010) Pumpkin eIF5A isoforms interact with components of the translational machinery in the cucurbit sieve tube system. Plant J 64:536–550

    Article  PubMed  CAS  Google Scholar 

  • Maffei ME, Mithofer A, Boland W (2007) Before gene expression: early events in plant–insect interaction. Trends Plant Sci 12:310–316

    Article  PubMed  CAS  Google Scholar 

  • Makandar R, Nalam V, Chaturvedi R, Jeannotte R, Sparks AA, Shah J (2010) Involvement of salicylate and jasmonate signaling pathways in Arabidopsis interaction with Fusarium graminearum. Mol Plant Microbe Interact 23:861–870

    Article  PubMed  CAS  Google Scholar 

  • Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419:399

    Article  PubMed  CAS  Google Scholar 

  • Malinowski R, Higgins R, Luo Y, Piper L, Nazir A, Bajwa V, Clouse S, Thompson P, Stratmann J (2009) The tomato brassinosteroid receptor BRI1 increases binding of systemin to tobacco plasma membranes, but is not involved in systemin signaling. Plant Mol Biol 70:603–616

    Article  PubMed  CAS  Google Scholar 

  • Mancuso S (1999) Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera. Aust J Plant Physiol 26:55–61

    Article  Google Scholar 

  • Manosalva PM, Park S-W, Forouhar F, Tong L, Fry WE, Klessig DF (2010) Methyl esterase 1 (StMES1) is required for systemic acquired resistance in potato. Mol Plant Microbe Interact 23:1151–1163

    Article  PubMed  CAS  Google Scholar 

  • Martin A, Adam H, Díaz-Mendoza M, Żurczak M, González-Schain ND, Suárez-López P (2009) Graft-transmissible induction of potato tuberization by the microRNA miR172. Development 136:2873–2881

    Article  PubMed  CAS  Google Scholar 

  • Mathieu J, Warthmann N, Küttner F, Schmid M (2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17:1055–1060

    Article  PubMed  CAS  Google Scholar 

  • Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956

    PubMed  CAS  Google Scholar 

  • Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol 137:149–156

    Article  PubMed  CAS  Google Scholar 

  • Miller AJ, Fan X, Shen Q, Smith SJ (2008) Amino acids and nitrate as signals for the regulation of nitrogen acquisition. J Exp Bot 59:111–119

    Article  PubMed  CAS  Google Scholar 

  • Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2:ra45

    Article  PubMed  Google Scholar 

  • Minchin PEH, Thorpe MR (1987) Measurement of unloading and reloading of photoassimilate within the stem of bean. J Exp Bot 38:211–220

    Article  Google Scholar 

  • Mishina TE, Zeier J (2007) Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J 50:500–513

    Article  PubMed  CAS  Google Scholar 

  • Misson J, Thibaud MC, Bechtold N, Raghothama K, Nussaume L (2004) Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants. Plant Mol Biol 55:727–741

    Article  PubMed  CAS  Google Scholar 

  • Montoya T, Nomura T, Farrar K, Kaneta T, Yokota T, Bishop GJ (2002) Cloning the tomato Curl3 gene highlights the putative dual role of the leucine-rich repeat receptor kinase tBRI1/SR160 in plant steroid hormone and peptide hormone signaling. Plant Cell 14:3163–3176

    Article  PubMed  CAS  Google Scholar 

  • Mudge SR, Rae AL, Diatloff E, Smith FW (2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant J 31:341–353

    Article  PubMed  CAS  Google Scholar 

  • Mullendore DL, Windt CW, Van As H, Knoblauch M (2010) Sieve tube geometry in relation to phloem flow. Plant Cell 22:579–593

    Article  PubMed  CAS  Google Scholar 

  • Muszynski MG, Dam T, Li B, Shirbroun DM, Hou Z, Bruggemann E, Archibald R, Ananiev EV, Danilevskaya ON (2006) Delayed flowering1 encodes a basic leucine zipper protein that mediates floral inductive signals at the shoot apex in maize. Plant Physiol 142:1523–1536

    Article  PubMed  CAS  Google Scholar 

  • Mutasa-Göttgens E, Hedden P (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 60:1979–1989

    Article  PubMed  CAS  Google Scholar 

  • Narváez-Vásquez J, Ryan C (2004) The cellular localization of prosystemin: a functional role for phloem parenchyma in systemic wound signaling. Planta 218:360–369

    Article  PubMed  CAS  Google Scholar 

  • Nelson T, Tausta SL, Gandotra N, Liu T (2006) Laser microdissection of plant tissue: what you see is what you get. Annu Rev Plant Biol 57:181–201

    Article  PubMed  CAS  Google Scholar 

  • Ohto M, Onai K, Furukawa Y, Aoki E, Araki T, Nakamura K (2001) Effects of sugar on vegetative development and floral transition in Arabidopsis. Plant Physiol 127:252–261

    Article  PubMed  CAS  Google Scholar 

  • Oparka KJ, Turgeon R (1999) Sieve elements and companion cells-traffic control centers of the phloem. Plant Cell 11:739–750

    PubMed  CAS  Google Scholar 

  • Orians C (2005) Herbivores, vascular pathways, and systemic induction: facts and artifacts. J Chem Ecol 31:2231–2242

    Article  PubMed  CAS  Google Scholar 

  • Orozco-Cardenas ML, Narvaez-Vasquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191

    PubMed  CAS  Google Scholar 

  • Palauqui JC, Elmayan T, Pollien JM, Vaucheret H (1997) Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 16:4738–4745

    Article  PubMed  CAS  Google Scholar 

  • Pant BD, Buhtz A, Kehr J, Scheible W-R (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738

    Article  PubMed  CAS  Google Scholar 

  • Park S-W, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–116

    Article  PubMed  CAS  Google Scholar 

  • Parker JE (2009) The quest for long-distance signals in plant systemic immunity. Sci Signal 2:pe31

    Article  PubMed  CAS  Google Scholar 

  • Peer WA, Blakeslee JJ, Yang H, Murphy AS (2011) Seven things we think we know about auxin transport. Mol Plant 4:487–504

    Article  PubMed  CAS  Google Scholar 

  • Peng M, Hannam C, Gu H, Bi Y-M, Rothstein SJ (2007) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. Plant J 50:320–337

    Article  PubMed  CAS  Google Scholar 

  • Périlleux C, Bernier G (2002) The control of flowering: do genetical and physiological approaches converge? In: O’Neill SD, Roberts JA (eds) Plant reproduction, vol 6. Sheffield Academic Press, Sheffield, pp 1–32

    Google Scholar 

  • Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJL, Nilsson O (2010) An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330:1397–1400

    Article  PubMed  CAS  Google Scholar 

  • Pnueli L, Gutfinger T, Hareven D, Ben-Naim O, Ron N, Adir N, Lifschitz E (2001) Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering. Plant Cell 13:2687–2702

    PubMed  CAS  Google Scholar 

  • Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Yoneyama K, Nogué F, Rameau C (2011) Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138:1531–1539

    Article  PubMed  CAS  Google Scholar 

  • Ragni L, Nieminen K, Pacheco-Villalobos D, Sibout R, Schwechheimer C, Hardtke CS (2011) Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expansion. Plant Cell 23:1322–1336

    Article  PubMed  CAS  Google Scholar 

  • Rahayu YS, Walch-Liu P, Neumann G, Römheld V, von Wirén N, Bangerth F (2005) Root-derived cytokinins as long-distance signals for NO3- -induced stimulation of leaf growth. J Exp Bot 56:1143–1152

    Article  PubMed  CAS  Google Scholar 

  • Ranjan A, Fiene G, Fackendahl P, Hoecker U (2011) The Arabidopsis repressor of light signaling SPA1 acts in the phloem to regulate seedling de-etiolation, leaf expansion and flowering time. Development 138:1851–1862

    Article  PubMed  CAS  Google Scholar 

  • Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A (2006) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci USA 103:19206–19211

    Article  PubMed  CAS  Google Scholar 

  • Rhodes JD, Thain JF, Wildon DC (1996) The pathway for systemic electrical signal conduction in the wounded tomato plant. Planta 200:50–57

    Article  CAS  Google Scholar 

  • Roberts K, Love AJ, Laval V, Laird J, Tomos AD, Hooks MA, Milner JJ (2007) Long-distance movement of Cauliflower mosaic virus and host defence responses in Arabidopsis follow a predictable pattern that is determined by the leaf orthostichy. New Phytol 175:707–717

    Article  PubMed  CAS  Google Scholar 

  • Rocher F, Chollet JF, Jousse C, Bonnemain JL (2006) Salicylic acid, an ambimobile molecule exhibiting a high ability to accumulate in the phloem. Plant Physiol 141:1684–1693

    Article  PubMed  CAS  Google Scholar 

  • Roldán M, Gómez-Mena C, Ruiz-García L, Salinas J, Martínez-Zapater JM (1999) Sucrose availability on the aerial part of the plant promotes morphogenesis and flowering of Arabidopsis in the dark. Plant J 20:581–590

    Article  PubMed  Google Scholar 

  • Rubin G, Tohge T, Matsuda F, Saito K, W-Rd S (2009) Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21:3567–3584

    Article  PubMed  CAS  Google Scholar 

  • Rustérucci C, Espunya MC, Díaz M, Chabannes M, Martínez MC (2007) S-nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol 143:1282–1292

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69

    Article  PubMed  CAS  Google Scholar 

  • Scheer JM, Ryan CA (2002) The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc Natl Acad Sci USA 99:9585–9590

    Article  PubMed  CAS  Google Scholar 

  • Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377

    Article  PubMed  CAS  Google Scholar 

  • Searle I, He Y, Turck F, Vincent C, Fornara F, Krober S, Amasino RA, Coupland G (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev 20:898–912

    Article  PubMed  CAS  Google Scholar 

  • Seskar M, Shulaev V, Raskin I (1998) Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiol 116:387–392

    Article  CAS  Google Scholar 

  • Shah J (2009) Plants under attack: systemic signals in defence. Curr Opin Plant Biol 12:459–464

    Article  PubMed  CAS  Google Scholar 

  • Shalit A, Rozman A, Goldshmidt A, Alvarez JP, Bowman JL, Eshed Y, Lifschitz E (2009) The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proc Natl Acad Sci USA 106:8392–8397

    Article  PubMed  CAS  Google Scholar 

  • Shannon S, Meeks-Wagner DR (1991) A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3:877–892

    PubMed  CAS  Google Scholar 

  • Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu F-F, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405

    Article  PubMed  CAS  Google Scholar 

  • Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11:445–458

    PubMed  CAS  Google Scholar 

  • Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci USA 97:3753–3758

    Article  PubMed  CAS  Google Scholar 

  • Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39:629–642

    Article  PubMed  CAS  Google Scholar 

  • Sibout R, Plantegenet S, Hardtke CS (2008) Flowering as a condition for xylem expansion in Arabidopsis hypocotyl and root. Curr Biol 18:458–463

    Article  PubMed  CAS  Google Scholar 

  • Sieburth LE, Lee D-K (2010) BYPASS1: how a tiny mutant tells a big story about root-to-shoot signaling. J Integr Plant Biol 52:77–85

    Article  PubMed  CAS  Google Scholar 

  • Sjölund RD (1997) The phloem sieve element: a river runs through it. Plant Cell 9:1137–1146

    Article  PubMed  Google Scholar 

  • Skøt L, Sanderson R, Thomas A, Skøt K, Thorogood D, Latypova G, Asp T, Armstead I (2011) Allelic variation in the perennial ryegrass FLOWERING LOCUS T gene is associated with changes in flowering time across a range of populations. Plant Physiol 155:1013–1022

    Article  PubMed  CAS  Google Scholar 

  • Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci USA 104:18842–18847

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13:66–71

    Article  PubMed  CAS  Google Scholar 

  • Stenzel I, Hause B, Maucher H, Pitzschke A, Miersch O, Ziegler J, Ryan CA, Wasternack C (2003) Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato—amplification in wound signalling. Plant J 33:577–589

    Article  PubMed  CAS  Google Scholar 

  • Sticher L, Mauch-Mani B, Métraux JP (1997) Systemic acquired resistance. Annu Rev Phytopathol 35:235–270

    Article  PubMed  CAS  Google Scholar 

  • Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2:178–186

    Article  PubMed  CAS  Google Scholar 

  • Stratmann JW (2003) Long distance run in the wound response—jasmonic acid is pulling ahead. Trends Plant Sci 8:247–250

    Article  PubMed  CAS  Google Scholar 

  • Suárez-López P (2005) Long-range signalling in plant reproductive development. Int J Dev Biol 49:761–771

    Article  PubMed  CAS  Google Scholar 

  • Suzuki H, Xia Y, Cameron R, Shadle G, Blount J, Lamb C, Dixon RA (2004) Signals for local and systemic responses of plants to pathogen attack. J Exp Bot 55:169–179

    Article  PubMed  CAS  Google Scholar 

  • Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39:792–796

    Article  PubMed  CAS  Google Scholar 

  • Takada S, Goto K (2003) TERMINAL FLOWER 2, an Arabidopsis homolog of HETEROCHROMATIN PROTEIN1, counteracts the activation of FLOWERING LOCUS T by CONSTANS in the vascular tissues of leaves to regulate flowering time. Plant Cell 15:2856–2865

    Article  PubMed  CAS  Google Scholar 

  • Takei K, Sakakibara H, Taniguchi M, Sugiyama T (2001) Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol 42:85–93

    Article  PubMed  CAS  Google Scholar 

  • Takei K, Takahashi T, Sugiyama T, Yamaya T, Sakakibara H (2002) Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. J Exp Bot 53:971–977

    Article  PubMed  CAS  Google Scholar 

  • Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a Protein is a mobile flowering signal in rice. Science 316:1033–1036

    Article  PubMed  CAS  Google Scholar 

  • Teper-Bamnolker P, Samach A (2005) The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell 17:2661–2675

    Article  PubMed  CAS  Google Scholar 

  • Thibaud M-C, Arrighi JF, Bayle V, Chiarenza S, Creff A, Bustos R, Paz-Ares J, Poirier Y, Nussaume L (2010) Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J 64:775–789

    Article  PubMed  CAS  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–665

    Article  PubMed  CAS  Google Scholar 

  • Thompson MV (2006) Phloem: the long and the short of it. Trends Plant Sci 11:26–32

    Article  PubMed  CAS  Google Scholar 

  • Thompson GA, Goggin FL (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J Exp Bot 57:755–766

    Article  PubMed  CAS  Google Scholar 

  • Thorpe MR, Ferrieri AP, Herth MM, Ferrieri RA (2007) 11C-imaging: methyl jasmonate moves in both phloem and xylem, promotes transport of jasmonate, and of photoassimilate even after proton transport is decoupled. Planta 226:541–551

    Article  PubMed  CAS  Google Scholar 

  • Thorpe MR, Furch ACU, Minchin PEH, Föller J, Van Bel AJE, Hafke JB (2010) Rapid cooling triggers forisome dispersion just before phloem transport stops. Plant Cell Environ 33:259–271

    Article  PubMed  CAS  Google Scholar 

  • Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci USA 104:1075–1080

    Article  PubMed  CAS  Google Scholar 

  • Truman WM, Bennett MH, Turnbull CGN, Grant MR (2010) Arabidopsis auxin mutants are compromised in systemic acquired resistance and exhibit aberrant accumulation of various indolic compounds. Plant Physiol 152:1562–1573

    Article  PubMed  CAS  Google Scholar 

  • Tsuji H, Taoka K-i, Shimamoto K (2011) Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Curr Opin Plant Biol 14:45–52

    Article  PubMed  CAS  Google Scholar 

  • Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Ann Rev Plant Biol 59:573–594

    Article  CAS  Google Scholar 

  • Turgeon R, Wolf S (2009) Phloem transport: cellular pathways and molecular trafficking. Ann Rev Plant Biol 60:207–221

    Article  CAS  Google Scholar 

  • Turnbull CGN, Booker JP, Leyser HMO (2002) Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J 32:255–262

    Article  PubMed  CAS  Google Scholar 

  • Umehara M, Hanada A, Magome H, Takeda-Kamiya N, Yamaguchi S (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 51:1118–1126

    Article  PubMed  CAS  Google Scholar 

  • Urbanus SL, Martinelli AP, Dinh QD, Aizza LCB, Dornelas MC, Angenent GC, Immink RGH (2010) Intercellular transport of epidermis-expressed MADS domain transcription factors and their effect on plant morphology and floral transition. Plant J 63:60–72

    PubMed  CAS  Google Scholar 

  • Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–1006

    Article  PubMed  CAS  Google Scholar 

  • van Bel AJ (2003a) The phloem, a miracle of ingenuity. Plant Cell Environ 26:125–149

    Article  Google Scholar 

  • van Bel AJ (2003b) Transport phloem: low profile, high impact. Plant Physiol 131:1509–1510

    PubMed  Google Scholar 

  • van Bel AJ, Gaupels F (2004) Pathogen-induced resistance and alarm signals in the phloem. Mol Plant Pathol 5:495–504

    Article  Google Scholar 

  • van Bel AJE, Knoblauch M, Furch ACU, Hafke JB (2011a) Questions on phloem biology. 1. Electropotential waves, Ca2+ fluxes and cellular cascades along the propagation pathway. Plant Sci 181:210–218

    Google Scholar 

  • van Bel AJE, Furch ACU, Hafke JB, Knoblauch M, Patrick JW (2011b) Questions on phloem biology. 2. Mass flow, molecular hopping, distribution patterns and macromolecular signalling. Plant Sci 181:325–330

    Google Scholar 

  • van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    Article  PubMed  Google Scholar 

  • Van Norman JM, Breakfield NW, Benfey PN (2011) Intercellular communication during plant development. Plant Cell 23:855–864

    Article  PubMed  CAS  Google Scholar 

  • Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutiérrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:4477–4482

    Article  PubMed  CAS  Google Scholar 

  • Vilaine F, Palauqui JC, Amselem J, Kusiak C, Lemoine R, Dinant S (2003) Towards deciphering phloem: a transcriptome analysis of the phloem of Apium graveolens. Plant J 36:67–81

    Article  PubMed  CAS  Google Scholar 

  • Vlot AC, Klessig DF, Park S-W (2008a) Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol 11:436–442

    Article  PubMed  CAS  Google Scholar 

  • Vlot AC, Liu P-P, Cameron RK, Park S-W, Yang Y, Kumar D, Zhou F, Padukkavidana T, Gustafsson C, Pichersky E, Klessig DF (2008b) Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J 56:445–456

    Article  PubMed  CAS  Google Scholar 

  • Voinnet O, Baulcombe DC (1997) Systemic signalling in gene silencing. Nature 389:553

    Article  PubMed  CAS  Google Scholar 

  • Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866

    Article  PubMed  CAS  Google Scholar 

  • Walz C, Juenger M, Schad M, Kehr J (2002) Evidence for the presence and activity of a complete antioxidant defence system in mature sieve tubes. Plant J 31:189–197

    Article  PubMed  CAS  Google Scholar 

  • Wang Y-Y, Tsay Y-F (2011) Arabidopsis nitrate transporter NRT1.9 is important in phloem nitrate transport. Plant Cell 23:1945–1957

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 17:1784–1790

    Article  PubMed  CAS  Google Scholar 

  • Wasternack C, Stenzel I, Hause B, Hause G, Kutter C, Maucher H, Neumerkel J, Feussner I, Miersch O (2006) The wound response in tomato—role of jasmonic acid. J Plant Physiol 163:297–306

    Article  PubMed  CAS  Google Scholar 

  • Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059

    Article  PubMed  CAS  Google Scholar 

  • Will T, van Bel AJ (2006) Physical and chemical interactions between aphids and plants. J Exp Bot 57:729–737

    Article  PubMed  CAS  Google Scholar 

  • Will T, Tjallingii WF, Thonnessen A, van Bel AJ (2007) Molecular sabotage of plant defense by aphid saliva. Proc Natl Acad Sci USA 104:10536–10541

    Article  PubMed  CAS  Google Scholar 

  • Will T, Kornemann SR, Furch ACU, Tjallingii WF, van Bel AJE (2009) Aphid watery saliva counteracts sieve-tube occlusion: a universal phenomenon? J Exp Bot 212:3305–3312

    CAS  Google Scholar 

  • Windt CW, Vergeldt FJ, Jager PAD, Van As H (2006) MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco. Plant Cell Environ 29:1715–1729

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Wang L, Baldwin I (2008) Methyl jasmonate-elicited herbivore resistance: does MeJA function as a signal without being hydrolyzed to JA? Planta 227:1161–1168

    Article  PubMed  CAS  Google Scholar 

  • Xia Y, Suzuki H, Borevitz J, Blount J, Guo Z, Patel K, Dixon RA, Lamb C (2004) An extracellular aspartic protease functions in Arabidopsis disease resistance signaling. EMBO J 23:980–988

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi A, Kobayashi Y, Goto K, Abe M, Araki T (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol 46:1175–1189

    Article  PubMed  CAS  Google Scholar 

  • Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2483

    PubMed  CAS  Google Scholar 

  • Yoneyama K, Takeuchi Y, Sekimoto H (2007) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225:1031–1038

    Article  PubMed  CAS  Google Scholar 

  • Yoo BC, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S, Lee YM, Lough TJ, Lucas WJ (2004) A systemic small RNA signaling system in plants. Plant Cell 16:1979–2000

    Article  PubMed  CAS  Google Scholar 

  • Yoo SJ, Chung KS, Jung SH, Yoo SY, Lee JS, Ahn JH (2010) BROTHER OF FT AND TFL1 (BFT) has TFL1-like activity and functions redundantly with TFL1 in inflorescence meristem development in Arabidopsis. Plant J 63:241–253

    Article  PubMed  CAS  Google Scholar 

  • Zeevaart JAD (2008) Leaf-produced floral signals. Curr Opin Plant Biol 11:541–547

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Zhou J-M (2010) Plant immunity triggered by microbial molecular signatures. Mol Plant 3:783–793

    Article  PubMed  CAS  Google Scholar 

  • Zhao M, Ding H, Zhu J-K, Zhang F, Li W-X (2011) Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol 190:906–915

    Article  PubMed  CAS  Google Scholar 

  • Zhu Q-H, Helliwell CA (2011) Regulation of flowering time and floral patterning by miR172. J Exp Bot 62:487–495

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann MR, Maischak H, Mithofer A, Boland W, Felle HH (2009) System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiol 149:1593–1600

    Article  PubMed  CAS  Google Scholar 

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Dinant, S., Suárez-López, P. (2012). Multitude of Long-Distance Signal Molecules Acting Via Phloem. In: Witzany, G., Baluška, F. (eds) Biocommunication of Plants. Signaling and Communication in Plants, vol 14. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-23524-5_6

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