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Sieve Elements: The Favourite Habitat of Phytoplasmas

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Phytoplasmas

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1875))

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Abstract

The sieve elements are the only plant compartments, where phytoplasmas can survive and propagate. Therefore, this chapter is focussed on the specific molecular and cell-biological properties of the sieve element. Sieve element-companion cell complexes arise from (pro)cambial mother cells induced by key genes known to be decisive for sieve-element differentiation. The special anatomy, cell biology, and plasma-membrane outfit of sieve elements allows them to act collectively as a tube system that is able to drive a mass flow against the flow induced by transpiration. Plasmodesmal corridors are vital for the translocation of photoassimilates and systemic signals and for survival of the enucleate sieve elements. Of paramount importance is the Ca2+-dependent gating of plasmodesmata by callose and proteins. Hence, some of the complex, regulatory mechanisms to maintain Ca2+ homoeostasis in sieve elements are presented. Finally, the peculiarities of the chemical and physical sieve-element environment offered to phytoplasmas are discussed.

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References

  1. Weintraub PG, Beanland L (2006) Insect vectors of phytoplasmas. Annu Rev Entomol 51:91–111

    Article  CAS  PubMed  Google Scholar 

  2. Hogenhout SA, Oshima K, Ammar ED et al (2008) Phytoplasmas: bacteria that manipulate plants and insects. Mol Plant Pathol 9:403–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bosco D, D’Amelio R (2010) Transmission specificity and competition of multiple phytoplasmas in the insect vector. In: Weintraub P, Jones P (eds) Phytoplasmas: genomes, plant hosts and vectors. CABI, Wallingford, pp 293–308

    Google Scholar 

  4. Contaldo N, Bertaccini A, Paltrinieri S et al (2012) Axenic culture of plant pathogenic phytoplasmas. Phytopathol Mediterr 51:607–617

    CAS  Google Scholar 

  5. Contaldo N, Satta E, Zambon Y et al (2016) Development and evaluation of different complex media for phytoplasma isolation and growth. J Microbiol Meth 127:105–110

    Article  CAS  Google Scholar 

  6. Van Bel AJE, Hafke JB (2005) Physiochemical determinants of phloem transport. In: Holbrook NM, Zwieniecki M (eds) Vascular transport in plants. Elsevier, Amsterdam, pp 19–44

    Google Scholar 

  7. Van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant Cell Environ 26:125–150

    Article  Google Scholar 

  8. Mähönen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, Helariutta Y (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of Arabidopsis root. Genes Dev 14:2938–2943

    Article  PubMed  PubMed Central  Google Scholar 

  9. Otero S, Helariutta Y (2017) Companion cells: a diamond in the rough. J Exp Bot 68:71–78

    Article  CAS  PubMed  Google Scholar 

  10. Esau K (1977) Anatomy of seed plants, 2nd edn. Wiley New York, Santa Barbara, London, Sydney, Toronto

    Google Scholar 

  11. Esau K, Thorsch J (1985) Sieve plate pores and plasmodesmata, the communication channels of the symplast: ultrastructural aspects and developmental relations. Am J Bot 72:1641–1653

    Article  Google Scholar 

  12. Evert R (1990) Dicotyledons. In: Behnke H-D, Sjolund RD (eds) Sieve elements: comparative structure, induction and development. Springer, Berlin, pp 103–137

    Chapter  Google Scholar 

  13. Van Bel AJE, Knoblauch M (2000) Sieve element and companion cell: the story of the comatose patient and the hyperactive nurse. Austral J Plant Physiol 27:477–487

    Google Scholar 

  14. Van Bel AJE, Hess P (2003) Phloemtransport. Kollektiver Kraftakt zweier Exzentriker. Biol Unserer Zeit 33:220–230

    Article  Google Scholar 

  15. Rodriguez-Villalon A (2016) Wiring a plant: genetic networks for phloem formation in Arabidopsis thaliana roots. New Phytol 210:45–50

    Article  CAS  PubMed  Google Scholar 

  16. Mouchel CF, Briggs GC, Hardtke CS (2004) Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the shoot. Genes Dev 18:700–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Truernit E, Bauby H, Belcram K et al (2012) OCTOPUS, a polarly localised membrane-associated protein, regulates phloem differentiation entry in Arabidopsis thaliana. Development 139:1306–1315

    Article  CAS  PubMed  Google Scholar 

  18. Rodriquez-Villalon A, Gujas B, Kang Y et al (2014) Molecular genetic framework for protophloem formation. Proc Natl Acad Sci U S A 111:11551–11556

    Article  CAS  Google Scholar 

  19. Depuydt S, Rodriquez-Villalon A, Santuari L et al (2013) Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLEA45 requires the receptor-like kinase BAM3. Proc Natl Acad Sci U S A 110:7074–7079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ruiz-Sola MA, Coiro M, Crivelli S et al (2017) OCTOPUS-LIKE 2, a novel player in Arabidopsis root and vascular development, reveals a key role for OCTOPUS family genes in root metaphloem sieve tube differentiation. New Phytol 216:1191–1204. https://doi.org/10.1111/nph.14751

    Article  CAS  PubMed  Google Scholar 

  21. Bonke M, Thitamadee S, Mähönen AP et al (2003) APL regulates vascular tissue identity in Arabidopsis. Nature 426:181–186

    Article  CAS  PubMed  Google Scholar 

  22. Furuta KM, Yadav SR, Lehesranta S et al (2014) Arabidopsis NAC45/86 direct sieve element morphogenesis culminating in enucleation. Science 345:933–937

    Article  CAS  PubMed  Google Scholar 

  23. Esau K (1969) The phloem. Borntraeger, Berlin (Encyclopedia of Plant Anatomy, vol 5.2)

    Google Scholar 

  24. Engleman E (1965) Sieve elements of Impatiens sultani. II. Developmental aspects. Ann Bot 29:103–104

    Article  Google Scholar 

  25. Patrick JW, Tyerman SD, van Bel AJE (2015) Long distance transport. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. Wiley, Cichester, pp 658–710

    Google Scholar 

  26. Esau K, Cronshaw J (1968) Plastids and mitochondria in the phloem of Cucurbita. Can J Bot 46:877–880

    Article  Google Scholar 

  27. Thorsch J, Esau K (1981) Changes in the endoplasmic reticulum during differentiation of a sieve element in Gossypium hirsutum. J Ultrastruct Res 74:183–194

    Article  CAS  PubMed  Google Scholar 

  28. Thorsch J, Esau K (1981) Nuclear degeneration and the association of endoplasmic reticulum with the nuclear envelope and microtubules in maturing sieve elements of Gossypium hirsutum. J Ultrastruct Res 74:195–204

    Article  CAS  PubMed  Google Scholar 

  29. Sjolund RD, Shih CY (1983) Freeze-fracture analysis of phloem structure in plant tissue cultures. I. The sieve element reticulum. J Ultrastruct Res 82:111–121

    Article  CAS  PubMed  Google Scholar 

  30. Ehlers K, Knoblauch M, van Bel AJE (2000) Ultrastructural features of well-preserved and injured sieve elements: minute clamps keep the phloem conduits free for mass flow. Protoplasma 214:80–92

    Article  Google Scholar 

  31. Patrick JW (1997) Phloem unloading. Sieve element unloading and post-sieve element transport. Annu Rev Plant Physiol Plant Mol Biol 28:165–190

    Google Scholar 

  32. Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Lett 581:2309–2317

    Article  CAS  PubMed  Google Scholar 

  33. Ayre BG (2011) Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol Plant 4:377–394

    Article  CAS  PubMed  Google Scholar 

  34. Milne RJ, Perroux MJ, Rae AL et al (2016) Sucrose transporter localization and function in phloem unloading in developing stems. Plant Physiol 173:1330–1341

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Julius BT, Leach KA, Tran TM et al (2017) Sugar transporters in plants: new insights and discoveries. Plant Cell Physiol 58:1442–1460

    Article  CAS  PubMed  Google Scholar 

  36. Tegeder M (2014) Transporters involved in source to sink partitioning of amino acids and ureides. J Exp Bot 65:1865–1878

    Article  CAS  PubMed  Google Scholar 

  37. Stanfield R, Hacke U, Laur J (2017) Are phloem sieve tubes leaky conduits supported by numerous aquaporins? Am J Bot 104:719–732

    Article  CAS  PubMed  Google Scholar 

  38. Thompson M, Zwieniecki M (2005) The role of potassium in long-distance transport in plants. In: Holbrook NM, Zwieniecki M (eds) Vascular transport in plants. Elsevier, Amsterdam, pp 221–240

    Chapter  Google Scholar 

  39. Dreyer I, Gomes-Porras JL, Riedelsberger J (2017) The potassium battery: a mobile energy source for transport processes in plant vascular tissues. New Phytol 216(4):1049–1053. https://doi.org/10.1111/nph.14667

    Article  PubMed  Google Scholar 

  40. Rogiers SY, Coetzee ZA, Walker RR et al (2017) Potassium in the grape (Vitis vinifera L.) berry: transport and function. Front Plant Sci 8:1629

    Article  PubMed  PubMed Central  Google Scholar 

  41. Thion L, Mazars C, Nacry P et al (1998) Plasma membrane depolarization activated calcium channels, stimulated by microtubule-depolymerizing drugs in wild-type Arabidopsis thaliana protoplasts, display constitutively large activities and a longer half-life in ton 2 mutant cells affected in the organization of cortical microtubules. Plant J 13:603–610

    Article  CAS  PubMed  Google Scholar 

  42. Hamilton DW, Hills A, Kohler B et al (2000) Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci U S A 97:4967–4972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. White PJ, Davenport RJ (2002) The voltage-independent cation channel in the plasma membrane of wheat roots is permeable to divalent cations and may be involved in cytosolic homeostasis. Plant Physiol 130:1386–1395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Furch ACU, van Bel AJE, Fricker MD et al (2009) Sieve element Ca2+ channels as relay stations between remote stimuli and sieve tube occlusion. Plant Cell 21:2118–2132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Van Bel AJE, Furch ACU, Will T et al (2014) Spread the news: systemic dissemination and local impact of Ca2+ signals along the phloem pathway. J Exp Bot 65:1761–1787

    Article  PubMed  CAS  Google Scholar 

  46. Van Bel AJE, Kempers R (1991) Symplastic isolation of the sieve element-companion cell complex in the phloem of Ricinus communis and Salix alba stems. Planta 183:69–76

    Article  PubMed  Google Scholar 

  47. Buvat R (1960) Observations sur l’infrastructure du cytoplasma au cours de la différenciation des cellules criblées de Cucurbita pepo L. C R Acad Sci 250:1528–1530

    Google Scholar 

  48. Behnke H-D (1965) Über das Phloem der Dioscoreaceen unter besonderer Berücksichtigung ihrer Phloembecken II Elektronenoptische Untersuchungen zur Feinstruktur des Phloembeckens. Z Pflanzenphysiol 53:214–244

    Google Scholar 

  49. Esau K, Cronshaw J (1968) Endoplasmic reticulum in the sieve element of Cucurbita. J Ultrastr Res 23:1–14

    Article  CAS  Google Scholar 

  50. Behnke HD (1991) Distribution and evolution of forms and types of sieve-element plastids in the dicotyledons. Aliso 3:167–182

    Article  Google Scholar 

  51. Parthasarathy MV, Pesacreta TC (1980) Microfilaments in plant vascular cells. Can J Bot 58:807–815

    Article  Google Scholar 

  52. Schobert C, Baker L, Szederkenyi J et al (1998) Identification of immunologically related proteins in sieve-tube exudate collected from monocotyledonous and dicotyledonous plants. Planta 206:245–252

    Article  CAS  Google Scholar 

  53. Schobert C, Gottschalk M, Kovar DR et al (2000) Characterization of Ricinus communis phloem profilin, RcPRO1. Plant Mol Biol 42:719–730

    Article  CAS  PubMed  Google Scholar 

  54. Kulikova AL, Puryaseva AP (2002) Actin in pumpkin phloem exudate. Russ J Plant Physiol 49:54–60

    Article  CAS  Google Scholar 

  55. Barnes A, Bale J, Constantinidou C et al (2004) Determining protein identity from sieve element sap in Ricinus communis L. by quadruple time of flight (Q-TOF) mass spectrometry. J Exp Bot 55:1473–1481

    Article  CAS  PubMed  Google Scholar 

  56. Walz C, Giavalisco P, Schad M et al (2004) Proteomics of cucurbit phloem exudate reveals a network of defence proteins. Phytochemistry 65:1795–1804

    Article  CAS  PubMed  Google Scholar 

  57. Giavalisco P, Kapitza K, Kolasa A et al (2006) Towards the proteome of Brassica napus phloem sap. Proteomics 6:896–909

    Article  CAS  PubMed  Google Scholar 

  58. Aki T, Shigyo M, Nakano R et al (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  CAS  PubMed  Google Scholar 

  59. Hafke JB, Ehlers K, Föller J et al (2013) Involvement of the sieve element cytoskeleton in electrical responses to cold shocks. Plant Physiol 162:707–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Furch ACU, Buxa SV, van Bel AJE (2015) Similar intracellular location and stimulus reactivity, but differential mobility of tailless (Vicia faba) and tailed forisomes (Phaseolus vulgaris) in intact sieve tubes. PLoS One 10:e0143920

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Cronshaw J, Sabnis DD (1990) Phloem proteins. In: Behnke H-D, Sjolund RD (eds) Sieve elements: comparative structure, induction and development. Springer, Berlin, pp 255–283

    Google Scholar 

  62. Furch ACU, Hafke JB, van Bel AJE (2008) Plant- and stimulus-specific variations in remote-controlled sieve-tube occlusion. Plant Sign Behav 3:858–861

    Article  Google Scholar 

  63. Rüping B, Ernst AM, Jekat SB et al (2010) Molecular and phylogenetic characterization of the sieve element occlusion family in Fabaceae and non-Fabaceae plants. BMC Plant Biol 10:219

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Anstead JA, Froelich DR, Knoblauch M et al (2012) Arabidopsis P-protein filament formation requires both AtSEO1 and AtSEO2. Plant Cell Physiol 53:1089–1094

    Article  CAS  Google Scholar 

  65. Batailler B, Lemaitre T, Vilaine F et al (2012) Soluble and filamentous proteins in Arabidopsis sieve elements. Plant Cell Environ 35:1258–1273

    Article  CAS  PubMed  Google Scholar 

  66. Knoblauch M, Ehlers K, Peters WS et al (2001) Reversible calcium-regulated stopcocks in legume sieve tubes. Plant Cell 13:1221–1230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Peters WS, Haffer D, Hanakam CB et al (2010) Legume phylogeny and the evolution of a unique contractile apparatus that regulates phloem transport. Am J Bot 97:797–808

    Article  PubMed  Google Scholar 

  68. Pélissier H, Peters WS, Collier R et al (2008) GFP tagging of sieve element occlusion (SEO) proteins results in green fluorescent forisomes. Plant Cell Physiol 49:1699–1710

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Froelich DR, Mullendore DL, Jensen KH et al (2011) Phloem ultrastructure and pressure flow: sieve-element-occlusion-related agglomerations do not affect translocation. Plant Cell 23:4428–4445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Ernst AM, Jekat SB, Zielonka S et al (2012) Sieve element occlusion (SEO) genes encode structural proteins involved in wound sealing of phloem. Proc Natl Acad Sci U S A 109:E1980–E1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Jekat SB, Ernst AM, von Bohl A et al (2013) P-proteins are heteromeric structures involved in rapid sieve tube sealing. Front Plant Sci 4:225

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Van Bel AJE, Will T (2016) Functional evaluation of proteins in watery and gel saliva of aphids. Front Plant Sci 7:1840

    PubMed  PubMed Central  Google Scholar 

  73. Pagliari L, Buoso S, Santi S et al (2017) Filamentous sieve element proteins are able to limit phloem mass flow, but not phytoplasma spread. J Exp Bot 68:3673–3688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Schobert C, Groβmann P, Gottschalk M et al (1995) Sieve-tube exudate from. Ricinus communis L. seedlings contains ubiquitin and chaperones. Planta 196:205–210

    Article  CAS  Google Scholar 

  75. Lin MK, Lee YJ, Lough TJ et al (2009) Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol Cell Proteomics 8:343–356

    Article  CAS  PubMed  Google Scholar 

  76. Ingvardsen C, Veierskov B (2001) Ubiquitin- and proteasome-dependent proteolysis in plants. Physiol Plant 112:451–459

    Article  CAS  PubMed  Google Scholar 

  77. Chavan RR, Braggins J, Harris PJ (2000) Companion cells in the secondary phloem of Indian dicotyledonous species: a quantitative study. New Phytol 146:107–118

    Article  Google Scholar 

  78. Kühn C, Franceschi VR, Schulz A et al (1997) Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275:1298–1300

    Article  PubMed  Google Scholar 

  79. Eschrich W, Heyser W (1975) Biochemistry of phloem constituents. In: Zimmermann MH, Milburn JA (eds) Encyclopedia of plant physiology. Transport in plants I Phloem transport. Springer, Heidelberg, pp 101–136

    Google Scholar 

  80. Szederkenyi J, Komor E, Schobert C (1997) Cloning of the cDNA glutaredoxin, an abundant sieve-tube exudate protein from Ricinus communis L and characterization of the glutathione-dependent thiol-reduction system in sieve tubes. Planta 202:349–356

    Article  CAS  PubMed  Google Scholar 

  81. Mullendore DL, Windt CW, van As H et al (2010) Sieve tube geometry in relation to phloem flow. Plant Cell 22:579–593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Bussières P (2014) Estimating the number and size of phloem sieve plate pores using longitudinal views and geometric reconstruction. Sci Rep 4:4929

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Barratt DH, Kolling K, Graf A et al (2011) Callose synthase GSL7 is necessary for normal phloem transport and inflorescence growth in Arabidopsis. Plant Physiol 155:328–341

    Article  CAS  PubMed  Google Scholar 

  84. Xie B, Wang X, Zhu M et al (2011) CalS7 encodes a callose synthase responsible for callose deposition in the phloem. Plant J 65:1–14

    Article  CAS  PubMed  Google Scholar 

  85. Vaten A, Dettmer J, Wu S et al (2011) Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell 21:1144–1155

    Article  CAS  PubMed  Google Scholar 

  86. Dettmer J, Ursache R, Campilho A et al (2014) CHOLINE TRANSPORTER-LIKE1 is required for sieve plate development to mediate long-distance cell-to-cell communication. Nat Commun 5:4276

    Article  CAS  PubMed  Google Scholar 

  87. Kraner ME, Link K, Melzer M et al (2017) Choline-transporter-like (CHER 1) is crucial for plasmodesmata maturation in Arabidopsis thaliana. Plant J 89:394–406

    Article  CAS  PubMed  Google Scholar 

  88. Deshpande BP (1975) Differentiation of the sieve plate of Cucurbita: a further view. Ann Bot 39:1015–1022

    Article  Google Scholar 

  89. Kempers R, Ammerlaan A, van Bel AJE (1998) Symplasmic constriction and ultrastructural features of the sieve element/companion cell complex in the transport phloem of apoplasmically and symplasmically phloem loading species. Plant Physiol 116:271–278

    Article  CAS  PubMed Central  Google Scholar 

  90. Lucas WJ, Groover A, Lichtenberger R et al (2013) The plant vascular system: evolution, development and functions. J Integr Plant Biol 55:294–388

    Article  CAS  PubMed  Google Scholar 

  91. Wasternack C, Hause B (2013) Jasmonate : biosynthesis, perception, signal transduction and. action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111:1021–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Campos ML, Kang J-H, Howe GA (2014) Jasmonate-triggered plant immunity. J Chem Ecol 40:657–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Das TA, Uddin M, Khan MMA et al (2015) Jasmonates counter plant stress: a review. Env Exp Bot 115:49–57

    Article  CAS  Google Scholar 

  94. Gilroy S, Bialasek M, Suzuki N et al (2016) ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol 171:1606–1615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Klessig DF, Tian M, Choi HW (2016) Multiple targets of salicylic acid and derivatives in plants and animals. Front Immunol 7:206

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Gaupels F, Durner J, Kogel K-H (2017) Production, amplification and systemic propagation of redox messengers in plants. The phloem can do it all! New Phytol 214:554–560

    Article  CAS  PubMed  Google Scholar 

  97. Wang N, Pierson EA, Setubal JC et al (2017) The candidatus Liberibacter-host interface: insights into pathogenesis mechanisms and disease control. Annu Rev Phytopathol 35:451–482

    Article  CAS  Google Scholar 

  98. Dempsey DA, Klessig DF (2012) SOS–too many signals for systemic acquired resistance? Trends Plant Sci 17:538–545

    Article  CAS  PubMed  Google Scholar 

  99. Shah J, Chaturvedi R, Chowdhury Z et al (2014) Signaling by small molecules in systemic acquired resistance. Plant Cell 79:645–658

    CAS  Google Scholar 

  100. Ham B-K, Lucas WJ (2017) Phloem-mobile RNAs as systemic signaling agents. Annu Rev Plant Biol 68:173–195

    Article  CAS  PubMed  Google Scholar 

  101. Thieme CJ, Rojas-Triana M, Stecyk E et al (2015) Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat Plants 1:15025

    Article  CAS  PubMed  Google Scholar 

  102. Yang Y, Mao L, Jittayasothorn Y et al (2015) Messenger RNA exchange between scions and rootstocks in grafted grapevines. BMC Plant Biol 15:251

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Zhang Z, Zheng Y, Ham B-K et al (2016) Vascular-mediated signalling involved in early phosphate stress response in plants. Nature Plants 2:16033

    Article  CAS  PubMed  Google Scholar 

  104. Yoo B-C, Kragler F, Varkonyi-Gasic E et al (2004) A systemic small RNA signaling system in plants. Plant Cell 16:1979–2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  106. Ham B-K, Li G, Jia W et al (2014) Systemic delivery of siRNA in pumpkin by a plant PHLOEM SMALL RNA-BINDING PROTEIN1–ribonucleoprotein complex. Plant J 80:683–694

    Article  CAS  PubMed  Google Scholar 

  107. Zhang W, Thieme CJ, Kollwig G et al (2016) t-RNA related sequences trigger mRNA transport in plants. Plant Cell 28:1237–1249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Taoka K, Ham B-K, Xoconostle-Cazares B et al (2007) Reciprocal phosphorylation and glycolysation recognition motifs control NCAPP1 interaction with pumpkin phloem proteins and their cell-to-cell movement. Plant Cell 19:1866–1884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Xoconostle-Cazares B, Xiang Y, Ruiz-Medrano R et al (1999) Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science 283:94–98

    Article  CAS  PubMed  Google Scholar 

  110. Lee J-Y, Yoo B-C, Rojas MR et al (2003) Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299:392–396

    Article  CAS  PubMed  Google Scholar 

  111. Lin MK, Belanger H, Lee YJ, Varkonyi-Gasic E et al (2007) FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell 19:1488–1506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Liu L, Liu C, Hou X et al (2012) FTIP1 is an essential regulator required for florigen transport. PLoS Biol 10:e1001313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Schulz A (2017) Long-distance trafficking: lost in transit or stopped at the gate? Plant Cell 29:426–430

    Article  PubMed  PubMed Central  Google Scholar 

  114. Paultre DSG, Gustin M-P, Molnar A et al (2016) Lost in transit: long-distance trafficking and phloem unloading of protein signals in Arabidopsis homografts. Plant Cell 28:2016–2025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Calderwood A, Kopriva S, Morris TJ (2016) Transcript abundance explains mRNA mobility data in Arabidopsis thaliana. Plant Cell 28:610–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Knoblauch M, van Bel AJE (1998) Sieve tubes in action. Plant Cell 10:35–50

    Article  CAS  PubMed Central  Google Scholar 

  117. Kauss H (1987) Some aspects of calcium-dependent regulation in plant metabolism. Annu Rev Plant Physiol 38:47–71

    Article  CAS  Google Scholar 

  118. Furch ACU, Hafke JB, Schulz A et al (2007) Calcium-mediated remote control of reversible sieve-tube occlusion in Vicia faba. J Exp Bot 28:2827–2838

    Article  CAS  Google Scholar 

  119. Furch ACU, Will T, Zimmermann MR et al (2010) Remote-controlled stop of mass flow in Cucurbita maxima. J Exp Bot 61:3697–3708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Hafke JB, Furch ACU, Fricker MD et al (2009) Forisome dispersion in Vicia faba is triggered by Ca2+ hotspots created by concerted action of diverse Ca2+ channels in sieve elements. Plant Sign Behav 4:968–972

    Article  CAS  Google Scholar 

  121. Tucker EB, Boss WF (1996) Mastoparan-induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiol 111:459–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Holdaway-Clarke TL, Walker NA, Hepler PK et al (2000) Physiological elevations in cytoplasmic free calcium or ion injection result in transient closure of higher plant plasmodesmata. Planta 210:329–335

    Article  CAS  PubMed  Google Scholar 

  123. Lee J-Y, Lu H (2011) Plasmodesmata: the battleground against intruders. Trends Plant Sci 16:201–210

    Article  CAS  PubMed  Google Scholar 

  124. Rinne PL, Welling A, Vahala J et al (2011) Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3 beta-glucanases to reopen signal conduits and release dormany in Populus. Plant Cell 23:130–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Zavaliev R, Ueki S, Epel BL et al (2011) Biology of callose (β-1,3 glucan) turnover at plasmodesmata. Protoplasma 249:117–130

    Article  CAS  Google Scholar 

  126. De Storme N, Geelen D (2014) Callose homeostasis at plasmodesmata: molecular regulators and developmental relevance. Front Plant Sci 5:138

    Article  PubMed  PubMed Central  Google Scholar 

  127. Kumar R, Kumar D, Hyun TK et al (2015) Players at plasmodesmal nano-channels. J Plant Biol 58:75–86

    Article  CAS  Google Scholar 

  128. Tilsner J, Nicolas W, Rosada A et al (2016) Staying tight: plasmodesmal membrane contact sites and the control of cell-to-cell connectivity. Annu Rev Plant Biol 67:337–364

    Article  CAS  PubMed  Google Scholar 

  129. Farrokhi N, Burton RA, Brownfield L et al (2006) Plant cell wall biosynthesis. Genetic, biochemical and functional genomics approach to the identification of key genes. Plant Biotech J 4:145–167

    Article  CAS  Google Scholar 

  130. Brownfield L, Ford K, Doblin MS et al (2007) Proteomic and chemical evidence links the callose synthase in Nicotiana alata pollen tubes to the product of the NASGL 1 gene. Plant J 52:147–156

    Article  CAS  PubMed  Google Scholar 

  131. Doxey AC, Yaish MWF, Moffatt BA et al (2007) Functional divergence in the Arabidopsis beta-1,3 glucanase family inferred by phylogenetic reconstruction of expression states. Mol Biol Evol 24:1045–1055

    Article  CAS  PubMed  Google Scholar 

  132. Amor Y, Haigler CH, Johnson S et al (1995) A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci U S A 92:9353–9357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Hong Z-L, Zhang Z-M, Olson JM et al (2001) A novel UDP-glucose transferase is part of the callose synthese complex and interacts with phragmoplastin at the forming cell plate. Plant Cell 13:769–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Musetti R, Buxa SV, De Marco F et al (2013) Phytoplasma-triggered Ca2+ influx is involved in sieve-tube blockage. Mol Plant-Micr Interact 26:379–386

    Article  CAS  Google Scholar 

  135. Tang R-J, Luan S (2017) Regulation of calcium and magnesium homeostasis in plants: from transporters to signaling network. Curr Opin Cell Biol 39:97–105

    Article  CAS  Google Scholar 

  136. Demidchik V, Maathuis FJM (2007) Physiological roles of non-selective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404

    Article  CAS  PubMed  Google Scholar 

  137. McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181:275–294

    Article  CAS  PubMed  Google Scholar 

  138. Pei Z-M, Murata Y, Benning G et al (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    Article  CAS  PubMed  Google Scholar 

  139. Nakagawa Y, Katagiri T, Shinozaki K et al (2007) Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots. Proc Natl Acad Sci U S A 104:3639–3644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Yamanaka T, Nakagawa Y, Mori K et al (2010) MCA1 and MCA2 that mediate Ca2+ uptake have distinct and overlapping roles in Arabidopsis. Plant Physiol 152:1284–1296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Hou C, Tian W, Kleist T et al (2014) DUF221 proteins are a family of osmosensitive calcium-permeable cation channels conserved across eukaryotes. Cell Res 24:632–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Yuan F, Yang H, Xue Y et al (2014) OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514:367–371

    Article  CAS  PubMed  Google Scholar 

  143. Clough SJ, Fengler KA, Yu I-C et al (2000) The Arabidopsis dnd1 ‘defense, no death’ gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci U S A 97:9323–9328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Gobert A, Park G, Amtmann A et al (2006) Arabidopsis thaliana cyclic nucleotide gated channel3 forms a non-selective ion transporter involved in germination and cation transport. J Exp Bot 57:791–800

    Article  CAS  PubMed  Google Scholar 

  145. Ali R, Ma W, Lemtiri-Chlieh F et al (2007) Death don’t have mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell 19:1081–1095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Gao F, Han X, Wu J et al (2012) A heat-activated calcium-permeable channel–Arabidopsis cyclic nucleotide ion channel 6–is involved in heat shock responses. Plant J 70:1056–1069

    Article  CAS  PubMed  Google Scholar 

  147. Mousavi SA, Chauvin A, Pascaud F et al (2013) GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500:422–426

    Article  CAS  PubMed  Google Scholar 

  148. Farmer EE, Gasperini D, Acosta IF (2014) The squeeze cell hypothesis for the activation of jasmonate synthesis in response to wounding. New Phytol 204:282–288

    Article  CAS  PubMed  Google Scholar 

  149. Vincill ED, Bieck AM, Spalding EP (2012) Ca2+ conduction by an amino acid-gated ion channel related to glutamate receptors. Plant Physiol 159:40–46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Evans MJ, Choi W-G, Gilroy S et al (2016) A ROS-assisted calcium wave dependent on the AtRBOHD NADPH oxidase and TPC1 cation channel propagates the systemic response to salt stress. Plant Physiol 171:1771–1784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Sze H, Liang F, Hwang I et al (2000) Diversity and regulation of plant Ca2+ pumps: insights from expression in yeast. Annu Rev Plant Physiol Plant Mol Biol 51:433–462

    Article  CAS  PubMed  Google Scholar 

  153. Frei dit Frey N, Mbuengue M, Kwaaitaal M et al (2012) Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development. Plant Physiol 159:798–809

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  154. Peiter E, Maathuis FJ, Mills L et al (2005) The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:404–408

    Article  CAS  PubMed  Google Scholar 

  155. Hedrich R, Marten I (2011) PPC1-SV channels gain shape. Mol Plant 4:426–441

    Article  CAS  Google Scholar 

  156. Choi W-G, Miller G, Wallace I et al (2017) Orhestrating rapid long-distance signaling in plants with Ca2+, ROS, and electrical signals. Plant J 90:698–707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620

    Article  CAS  PubMed  Google Scholar 

  158. Schumaker KS, Sze H (1985) A Ca2+/H+ antiport system driven by the proton electrochemical gradient of a tonoplast H+-ATPase from oat roots. Plant Physiol 79:1111–1117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Hirschi KD, Zhen RG, Cunningham KW et al (1996) CAX1, an H+/Ca2+ antiporter family from Arabidopsis. Proc Natl Acad Sci U S A 93:8782–8786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Cheng N-H, Pittman JK, Shigaki T et al (2005) Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homoiostasis. Plant Physiol 138:2948–2060

    Article  CAS  Google Scholar 

  161. Wang Y, Kang Y, Ma CX et al (2017) CNGC2 is a Ca2+ influx channel that prevents accumulation of apoplastic Ca2+ in the leaf. Plant Physiol 173:1342–1354

    Article  CAS  PubMed  Google Scholar 

  162. Gilroy S, Suzuki N, Miller G et al (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19:623–630

    Article  CAS  PubMed  Google Scholar 

  163. Takeda S, Gapper C, Kaya H et al (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–1244

    Article  CAS  PubMed  Google Scholar 

  164. Kimura S, Kaya H, Kawarazaki T et al (2012) Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim Biophys Acta 1823:398–405

    Article  CAS  PubMed  Google Scholar 

  165. Dubiella U, Seybold H, Durian G et al (2013) Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci U S A 110:8744–8749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Demidchik V, Shabala SN, Davies JN (2007) Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels. Plant J 47:377–386

    Article  CAS  Google Scholar 

  167. Garcia-Mata C, Wang J, Gajdanowicz P et al (2010) A minimal cysteine motif required to activate the SKOR K+ channel of Arabidopsis by the reactive oxygen species H2O2. J Biol Chem 285:29286–29294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Richards SI, Laohavisit A, Mortimer JC et al (2014) Annexin 1 regulates the H2O2-induced calcium signature in Arabidopsis thaliana roots. Plant J 77:136–145

    Article  CAS  PubMed  Google Scholar 

  169. Allen GJ, Chu S-P, Schumacher K, Shimazaki CT et al (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det2 mutant. Science 289:2338–2342

    Article  CAS  PubMed  Google Scholar 

  170. Minchin PEH, Thorpe ME (1987) Measurement of unloading and reloading of photo-assimilate within the stem of bean. J Exp Bot 38:211–220

    Article  Google Scholar 

  171. Van Bel AJE (1993) The transport phloem: specifics of its functioning. Prog Bot 54:134–150

    Google Scholar 

  172. 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 l 131:1519–1528

    Google Scholar 

  173. Hafke JB, van Amerongen JK, Kelling F et al (2005) Thermodynamic battle for photosynthate acquisition between sieve tubes and adjoining parenchyma in transport phloem. Plant Physiol 138:1527–1537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Minchin PEH, Lacointe A (2017) Consequences of phloem pathway unloading/reloading on equilibrium flows between source and sink: a modelling approach. Funct Plant Biol 44:507–514

    Article  PubMed  Google Scholar 

  175. Carpaneto A, Geiger D, Bamberg E et al (2005) Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under control of sucrose gradient and pmf. J Biol Chem 280:21437–21443

    Article  CAS  PubMed  Google Scholar 

  176. Schulte-Baukloh C, Fromm J (1993) The effect of calcium starvation on assimilate partitioning and mineral distribution of the phloem. J Exp Bot 44:1703–1707

    Article  CAS  Google Scholar 

  177. Van Bel AJE, Furch ACU, Hafke JB et al (2011) (Questions)n on phloem biology. 2. Mass flow, molecular hopping, distribution patterns and molecular signalling. Plant Sci 181:325–330

    Article  PubMed  CAS  Google Scholar 

  178. Fisher DB, Wu K, Ku MSB (1992) Turnover of soluble proteins in the wheat sieve tube. Plant Physiol 100:587–592

    Article  Google Scholar 

  179. Golecki B, Schulz A, Castens-Behrens U et al (1998) Evidence for graft transmission of structural proteins in heterografts of Cucurbitaceae. Planta 206:630–640

    Article  CAS  Google Scholar 

  180. Golecki B, Schulz A, Thompson GA (1999) Translocation of structural P-proteins in the phloem. Plant Cell 11:127–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Foster TM, Lough TJ, Emerson SJ et al (2002) A surveillance system regulates selective entry of RNA into the shoot apex. Plant Cell 14:1497–1508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. 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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  184. Rocher F, Chollet J-F, Jousse C et al (2006) Salicylic acid, an ambimobile molecule exhibiting a high ability to accumulate in the phloem. Plant Physiol 141:1684–1693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Aoki K, Suzui N, Fujimaki S et al (2005) Destination-selective long-distance movement of phloem proteins. Plant Cell 17:1801–1814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Biles CL, Abeles FB (1991) Xylem sap proteins. Plant Physiol 96:597–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Buhtz A, Kolasa A, Arlt K et al (2004) Xylem protein composition is conserved among different plant species. Planta 219:610–618

    Article  CAS  PubMed  Google Scholar 

  188. Kehr J, Buhtz A, Giavalisco P (2005) Analysis of xylem sap proteins from Brassica napus. BMC Plant Biol 5:11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  189. Rogers S, Peel AJ (1975) Some evidence for the existence of turgor pressure gradients in the sieve tube of willow. Planta 126:259–267

    Article  CAS  PubMed  Google Scholar 

  190. Vreugdenhil D, Koot-Gronsveld EAM (1989) Measurements of pH, sucrose and potassium ions in the phloem sap of castor bean (Ricinus communis) plants. Physiol Plant 77:385–388

    Article  CAS  Google Scholar 

  191. Minchin PEH, Ryan KG, Thorpe MR (1984) Further evidence of apoplastic unloading into the stem of bean: identification of the phloem buffering pool. J Exp Bot 35:1744–1753

    Article  Google Scholar 

  192. Gould N, Thorpe MR, Koroleva O et al (2005) Phloem hydrostatic pressure relates to solute loading rate: a direct test of the Münch hypothesis. Funct Plant Biol 32:1019–1026

    Article  PubMed  Google Scholar 

  193. Kimmerer TW, Stringer MA (1988) Alcohol dehydrogenase and ethanol in the stems of trees. Evidence for anaerobic metabolism in the vascular cambium. Plant Physiol 87:693–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. Van Dongen JT, Schurr U, Pfister M et al (2003) Phloem metabolism and function have to cope with low internal oxygen. Plant Physiol 131:1529–1543

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  195. Carvalho MR, Turgeon R, Owens T et al (2017) The scaling of the hydraulic architecture in poplar leaves. New Phytol 214:145–157

    Article  CAS  PubMed  Google Scholar 

  196. Esau K, Cheadle VI (1959) Size of pores and their contents in sieve elements of dicotyledons. Proc Natl Acad Sci U S A 45:156–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Trip P, Colvin JR (1970) Sieve elements of minor veins in the leaves of Beta vulgaris. Ann Bot 34:1101–1106

    Article  Google Scholar 

  198. Milburn JA (1970) Phloem exudate from castor bean: induction by massage. Planta 95:272–276

    Article  CAS  PubMed  Google Scholar 

  199. Smith JAC, Milburn JA (1980) Osmoregulation and the control of phloem-sap composition in Ricinus communis L. Planta 128:28–34

    Article  Google Scholar 

  200. Hocking PJ (1980) The composition of phloem exudate and xylem sap from tree tobacco (Nicotiana glauca Grah.). Ann Bot 45:633–643

    Article  CAS  Google Scholar 

  201. Fukumorita T, Chino M (1982) Sugar, amino acid and inorganic contents in rice phloem sap. Plant Cell Physiol 23:273–283

    CAS  Google Scholar 

  202. Fisher DB, Frame JF (1984) A guide to the use of the exuding-stylet technique in phloem physiology. Planta 161:385–393

    Article  CAS  PubMed  Google Scholar 

  203. Hayashi H, Chino M (1986) Collection of pure phloem sap from wheat and its chemical composition. Plant Cell Physiol 27:1387–1393

    Article  CAS  Google Scholar 

  204. Ohshima T, Hayashi H, Chino M (1990) Collection and chemical composition of pure phloem sap from Zea mays L. Plant Cell Physiol 31:735–737

    CAS  Google Scholar 

  205. Weibull J, Ronquist F, Brishammer S (1990) Free amino acid composition of leaf exudates and phloem sap. A comparative study in oats and barley. Plant Physiol 92:222–226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. Girousse C, Bonnemain J-L, Delrot S et al (1991) Sugar and amino acid composition of phloem sap of Medicago sativa: a comparative study of two collecting methods. Plant Physiol Biochem 29:41–48

    CAS  Google Scholar 

  207. Van Helden M, Tjallingii WF, van Beek TA (1994) Phloem sap collection from lettuce (Lactuca sativa L.): chemical composition among collection methods. J Chem Ecol 20:3191–3206

    Article  PubMed  Google Scholar 

  208. King RW, Zeevaart JAD (1974) Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiol 53:96–103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  209. Richardson PT, Baker DA (1982) The chemical composition of cucurbit vascular exudates. J Exp Bot 33:1239–1247

    Article  CAS  Google Scholar 

  210. Hayashi H, Chino M (1990) Chemical composition of phloem sap from the uppermost internode of the rice plant. Plant Cell Physiol 31:247–251

    CAS  Google Scholar 

  211. Leckstein PM, Llewellyn M (1975) Quantitative analysis of seasonal variation in the amino acids in phloem sap of Salix alba L. Planta 124:89–91

    Article  CAS  PubMed  Google Scholar 

  212. Felle H, Bertl A (1986) The fabrication of H+-selective liquid membrane microelectrodes for use in plant cells. J Exp Bot 37:1416–1428

    Article  CAS  Google Scholar 

  213. Felle H (2001) pH: signal and messenger in plants cells. Plant Biol 3:577–591

    Article  CAS  Google Scholar 

  214. Frohmeyer H, Grabov A, Blatt MR (1998) A role for the vacuole in auxin-mediated control of cytosolic pH in Vicia mesophyll and guard cells. Plant J 13:109–116

    Article  Google Scholar 

  215. Hafke JB, Neff R, Hütt M-T et al (2001) Day-to-night variations of cytoplasmic pH in a crassulacean acid metabolism plant. Protoplasma 216:164–170

    Article  CAS  PubMed  Google Scholar 

  216. Bertaccini A, Duduk B, Paltrinieri S et al (2014) Phytoplasmas and phytoplasma diseases: a severe threat to agriculture. Am J Plant Sci 5:1763–1788

    Article  Google Scholar 

  217. Wei W, Kakizawa S, Suzuki S et al (2004) In planta dynamic analysis of onion yellows phytoplasma using localized inoculation by insect transmission. Phytopathology 94:244–250

    Article  PubMed  Google Scholar 

  218. Buxa SV, Degola F, Polizzotto R et al (2015) Phytoplasma infection in tomato is associated with re-organization of plasma membrane, ER stacks and actin filaments in sieve elements. Front Plant Sci 6:650

    Article  PubMed  PubMed Central  Google Scholar 

  219. Musetti R, Pagliari L, Buxa SV et al (2016) OHMS: phytoplasmas dictate changes in sieve-element ultrastructure to accommodate their requirements for nutrition, multiplication and translocation. Plant Sign Behav 11:e1138191

    Article  CAS  Google Scholar 

  220. Kube M, Morovic J, Duduk B et al (2012) Current view on phytoplasma genomes and encoded metabolism. Sci World J 2012:185942

    Article  CAS  Google Scholar 

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van Bel, A.J.E. (2019). Sieve Elements: The Favourite Habitat of Phytoplasmas. In: Musetti, R., Pagliari, L. (eds) Phytoplasmas. Methods in Molecular Biology, vol 1875. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-8837-2_19

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