Abstract
Cucurbit phloem is especially interesting and unusual in several respects, which has made these plants the subject of intensive study by microscopists, physiologists and molecular biologists. Early light microscopists were attracted to cucurbits due to the large dimensions of the sieve tubes and sieve pores, which made them relatively easy to see (Esau, The phloem. Berlin/Stuttgart: Gebrüder Borntraeger, 1969). Hartig, the forest botanist who discovered the sieve element, turned to Cucurbita in his studies, describing many aspects of phloem structure including sieve plates, callose and “slime plugs.” (See Esau, The phloem. Berlin/Stuttgart: Gebrüder Borntraeger, 1969 for the early history of phloem research). Cucurbita has also featured strongly in the analysis of phloem development. For example, Esau et al. (Bot Gaz 123:233–243, 1962) described the development of the sieve pores and the involvement of callose deposition in this process in Cucurbita maxima. A striking feature of cucurbit phloem is the presence of a unique array of extrafascicular (outside the vascular bundles) sieve tubes, which have been studied by several groups in recent years (Zhang et al. Proc Nat Acad Sci U S A 107:13532–13537, 2010; Gaupels et al. Plant Physiol 160:2285–2299, 2012; Zhang et al. Plant Physiol 158:1873–1882, 2012; Gaupels and Ghirardo, Front Plant Sci 4:187, 2013; Gaupels et al. Front Plant Sci 7:154, 2016).
Another interesting quirk is that cucurbit “phloem” exudes copiously when cut, which has led to its use in many metabolomic and proteomic analyses. It should be noted, however, that as early as 1944 Crafts and Lorenz thought the high nitrogen content of cucurbit exudate so unusual as to make it suspect as true, mobile phloem sap, a caution that has borne out in recent years (see below). In this chapter I will leave much of the early history of cucurbit phloem biology to Esau (The phloem. Berlin/Stuttgart: Gebrüder Borntraeger, 1969) and focus for the most part on several aspects of the subject addressed since the publication of her monumental work.
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References
Alosi MC, Melroy DL, Park RB. The regulation of gelation of phloem exudate from Cucurbita fruit by dilution, glutathione, and glutathione reductase. Plant Physiol. 1988;86:1089–94.
Anandan A, Gatehouse LN, Marshall RK, Murray C, Christeller JT. Two highly homologous promoters of a squash aspartic protease inhibitor (SQAPI) multigene family exhibit differential expression in transgenic tobacco phloem and trichome cells. Plant Mol Biol Report. 2009;27:355–64.
Anstead JA, Froelich DR, Knoblauch M, Thompson GA. Arabidopsis P-protein filament formation requires both AtSEOR1 and AtSEOR2. Plant Cell Physiol. 2012;53:1033–42.
Balachandran S, Xiang Y, Schobert C, Thompson GA, Lucas WJ. Phloem sap proteins from Cucurbita maxima and Ricinus communis have the capacity to traffic cell to cell through plasmodesmata. Proc Natl Acad Sci U S A. 1997;94:14150–5.
Beyenbach J, Weber C, Kleinig H. Sieve-tube proteins from Cucurbita maxima. Planta. 1974;119:113–24.
Bobbili KB, Bandari S, Grobe K, Swamy MJ. Mutational analysis of the pumpkin (Cucurbita maxima) phloem exudate lectin, PP2 reveals Ser-104 is crucial for carbohydrate binding. Biochem Biophys Res Commun. 2014;450:622–7.
Bostwick DE, Dannenhoffer JM, Skaggs MI, Lister RM, Larkins BA, Thompson GA. Pumpkin phloem lectin genes are specifically expressed in companion cells. Plant Cell. 1992;4:1539–48.
Christeller JT, Farley PC, Marshall RK, Anandan A, Wright MM, Newcomb RD, et al. The squash aspartic proteinase inhibitor SQAPI is widely present in the Cucurbitales, comprises a small multigene family, and is a member of the phytocystatin family. J Mol Evol. 2006;63:747–57.
Christeller JT, Farley PC, Ramsay RJ, Sullivan PA, Laing WA. Purification, characterization and cloning of an aspartic proteinase inhibitor from squash phloem exudate. Eur J Biochem. 1998;254:160–7.
Clark AM, Jacobsen KR, Bostwick DE, Dannenhoffer JM, Skaggs MI, Thompson GA. Molecular characterization of a phloem-specific gene encoding the filament protein, Phloem Protein 1 (PP1), from Cucurbita maxima. Plant J. 1997;12:49–61.
Crafts AS. Phloem anatomy, exudation, and transport of organic nutrients in cucurbits. Plant Physiol. 1932;7:i4.
Cronshaw J, Esau K. P protein in the phloem of Cucurbita II. The P protein of mature sieve elements. J Cell Biol. 1968;38:292–303.
Cronshaw J, Sabnis DD. Phloem proteins. In: Sieve elements. Comparative structure, induction and development. Berlin: Springer; 1990. p. 257–83.
Dannenhoffer JM, Schulz A, Skaggs MI, Bostwick DE, Thompson GA. Expression of the phloem lectin is developmentally linked to vascular differentiation in cucurbits. Planta. 1997;201:405–14.
Davidson A, Keller F, Turgeon R. Phloem loading, plant growth form, and climate. Protoplasma. 2011;248:153–63.
De Schepper V, De Swaef T, Bauweraerts I. Kathy Phloem transport: a review of mechanisms and controls. J Exp Bot. 2013;64:4839–50.
Dinant S, Clark AM, Zhu Y, Vilaine F, JC P, Kusiak C, et al. Diversity of the superfamily of phloem lectins (phloem protein 2) in angiosperms. Plant Physiol. 2003;131:114–28.
Dölger J, Rademaker H, Liesche J, Schulz A, Bohr T. Diffusion and bulk flow in phloem loading: a theoretical analysis of the polymer trap mechanism for sugar transport in plants. Phys Rev E. 2014;90:042704.
Ernst AM, Jekat SB, Zielonka S, Müller B, Neumann U, Rüping B, et al. Sieve element occlusion (SEO) genes encode structural phloem proteins involved in wound sealing of the phloem. Proc Natl Acad Sci U S A. 2012;109:E1980–9.
Ernst AM, Rüping B, Jekat SB, Nordzieke S, Reineke AR, Müller B, et al. The sieve element occlusion gene family in dicotyledonous plants. Plant Signal Behav. 2011;6:151–3.
Esau K. The Phloem. Berlin/Stuttgart: Gebrüder Borntraeger; 1969.
Eschrich W. Beziehungen zwischen dem Auftreten von Callose und der Feinstruktur des primären Phloems bei Cucurbita ficifolia. Planta. 1963;59:243–61.
Eschrich W. Biochemistry and fine structure of phloem in relation to transport. Annu Rev Plant Physiol. 1970;21:193–214.
Evert RF, Eschrich W, Eichhorn SE. P-protein distribution in mature sieve elements of Cucurbita maxima. Planta. 1972;109:193–210.
Fisher D. Ultrastructure, plasmodesmatal frequency, and solute concentration in green areas of variegated Coleus blumei Benth leaves. Planta. 1986;169:141–52.
Froelich DR, Mullendore DL, Jensen KH, Ross-Elliott TJ, Anstead JA, Thompson GA, et al. Phloem ultrastructure and pressure flow: sieve-element-occlusion-related agglomerations do not affect translocation. Plant Cell. 2011;23:4428–45.
Furch AC, van Bel AJ, Will T. Aphid salivary proteases are capable of degrading sieve-tube proteins. J Exp Bot. 2014;66:533–9.
Furch AC, Zimmermann MR, Will T, Hafke JB, Van Bel AJ. Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima. J Exp Bot. 2010. doi:10.1093/jxb/erq181.
Gaupels F, Furch AC, Zimmermann MR, Chen F, Kaever V, Buhtz A, et al. Systemic induction of NO-, redox-, and cGMP signaling in the pumpkin extrafascicular phloem upon local leaf wounding. Front Plant Sci. 2016;7:154.
Gaupels F, Ghirardo A. The extrafascicular phloem is made for fighting. Front Plant Sci. 2013;4:187.
Gaupels F, Sarioglu H, Beckmann M, Hause B, Spannagl M, Draper J, et al. Deciphering systemic wound responses of the pumpkin extrafascicular phloem by metabolomics and stable isotope-coded protein labeling. Plant Physiol. 2012;160:2285–99.
Golecki B, Schulz A, Carstens-Behrens U, Kollmann R. Evidence for graft transmission of structural phloem proteins or their precursors in heterografts of Cucurbitaceae. Planta. 1998;206:630–40.
Golecki B, Schulz A, Thompson GA. Translocation of structural P proteins in the phloem. Plant Cell. 1999;11:127–40.
Gómez G, Pallás V. Identification of an in vitro ribonucleoprotein complex between a viroid RNA and a phloem protein from cucumber plants. Mol Plant Microbe Interact. 2001;14:910–3.
Gowan E, Lewis BA, Turgeon R. Phloem transport of antirrhinoside, an iridoid glycoside, in Asarina scandens (Scrophulariaceae). J Chem Ecol. 1995;21:1781–8.
Jeffrey C. A review of the Cucurbitaceae. Bot J Linn Soc. 1980;81:233–47.
Jekat SB, Ernst AM, von Bohl A, Zielonka S, Twyman RM, Noll GA, et al. P-proteins in Arabidopsis are heteromeric structures involved in rapid sieve tube sealing. Front Plant Sci. 2013;4:225.
Kehr J. Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. J Exp Bot. 2006;57:767–74.
Kleinig H, Thönes J, Dörr I, Kollmann R. Filament formation in vitro of a sieve tube protein from Cucurbita maxima and Cucurbita pepo. Planta. 1975;127:163–70.
Knoblauch M, Froelich DR, Pickard WF, Peters WS. SEORious business: structural proteins in sieve tubes and their involvement in sieve element occlusion. J Exp Bot. 2014. doi:10.1093/jxb/eru071.
Knoblauch M, Peters WS, Ehlers K, van Bel AJ. Reversible calcium-regulated stopcocks in legume sieve tubes. Plant Cell. 2001;13:1221–30.
Knoblauch M, van Bel AJE. Sieve tubes in action. Plant Cell. 1998;10:35–50.
Knop C, Stadler R, Sauer N, Lohaus G. AmSUT1, a sucrose transporter in collection and transport phloem of the putative symplastic phloem loader Alonsoa meridionalis. Plant Physiol. 2004;134:2040214.
Kollmann R, Dörr I, Kleinig H. Protein filaments-structural components of the phloem exudate. I. Observations with Cucurbita and Nicotiana. Planta. 1970;95:86–94.
Konno K. Plant latex and other exudates as plant defense systems: roles of various defense chemicals and proteins contained therein. Phytochemistry. 2011;72:1510–30.
Leineweber K, Schulz A, Thompson GA. Dynamic transitions in the translocated phloem filament protein. Funct Plant Biol. 2000;27:733–41.
Liesche J, Schulz A. Symplasmic transport in phloem loading and unloading. In: Sokolowska K, Sowiński P, editors. Symplasmic transport in vascular plants. New York: Springer Science+ Business Media; 2013. p. 133–63.
Lin MK, Lee YJ, Lough TJ, Phinney BS, Lucas WJ. Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol Cell Proteomics. 2009;8:343–56.
Mullendore DL, Windt CW, Van As H, Knoblauch M. Sieve tube geometry in relation to phloem flow. Plant Cell. 2010;22:579–93.
Murray C, Christeller JT. Purification of a trypsin inhibitor (PFTI) from pumpkin fruit phloem exudate and isolation of putative trypsin and chymotrypsin inhibitor cDNA clones. Biol Chem Hoppe Seyler. 1995;376:281–8.
Öener-Sieben S, Rappi C, Sauer N, Stadler R, Lohaus G. Characterization, localization, and seasonal changes of the sucrose trasnporter FeSUT1 in the phloem of Fraxinus excelsior. J Exp Bot. 2015;66:4807–19.
Oparka KJ, Turgeon R. Sieve elements and companion cells-traffic control centers of the phloem. Plant Cell. 1999;11:739–50.
Owens R, Blackburn M, Ding B. Possible involvement of the phloem lectin in long-distance viroid movement. Mol Plant Microbe Interact. 2001;14:905–9.
Read S, Northcote D. Chemical and immunological similarities between the phloem proteins of three genera of the Cucurbitaceae. Planta. 1983a;158:119–27.
Read SM, Northcote DH. Subunit structure and interactions of the phloem proteins of Cucurbita maxima (pumpkin). Eur J Biochem. 1983b;134:561–9.
Richardson PT, Baker DA. The chemical composition of cucurbit vascular exudates. J Exp Bot. 1982;33:1239–47.
Sabnis D, Hart J. The isolation and some properties of a lectin (haemagglutinin) from Cucurbita phloem exudate. Planta. 1978;142:97–101.
Sabnis DD, Hart JW. A comparative analysis of phloem exudate proteins from Cucumis melo, Cucumis sativus and Cucurbita maxima by polyacrylamide gel electrophoresis and isoelectric focusing. Planta. 1976;130:211–8.
Sabnis DD, Hart JW. Heterogeneity in phloem protein complements from different species. Planta. 1979;145:459–66.
Savage JA, Clearwater MJ, Haines DF, Klein T, Mencuccini M, Sevanto S, et al. Allocation, stress tolerance and carbon transport in plants: how does phloem physiology affect plant ecology? Plant Cell Environ. 2015. doi:10.1111/pce.12602.
Savage JA, Zwieniecki MA, Holbrook NM. Phloem transport velocity varies over time and among vascular bundles during early cucumber seedling development. Plant Physiol. 2013;163:1409–18.
Schaefer H, Renner SS. Phylogenetic relationships in the order Cucurbitales and a new classification of the gourd family (Cucurbitaceae). Taxon. 2011;60:122–38.
Shah J, Jacob R. Development and structure of phloem in the petiole of Lagenaria siceraria (Mol.) Standl. and Momordica charantia L. Ann Bot. 1969;33:855–63.
Slewinski TL, Zhang C, Turgeon R. Structural and functional heterogeneity in phloem loading and transport. Front Plant Sci. 2013;4:1–11.
Smith LM, Sabnis DD, Johnson RP. Immunocytochemical localisation of phloem lectin from Cucurbita maxima using peroxidase and colloidal-gold labels. Planta. 1987;170:461–70.
Sui X, Meng F, Wang H, Wei Y, Li R, Wang Z, et al. Molecular cloning, characteristics and low temperature response of raffinose synthase gene in Cucumis sativus L. J Plant Physiol. 2012;169:1883–91.
Tolstikov V, Fiehn O, Tanaka N. Application of liquid chromatography-mass spectrometry analysis in metabolomics. In: Metabolomics: methods and protocols, methods in molecular biology, vol. 358. Totowa: Humana; 2007. p. 141–55.
Turgeon R, Beebe DU, Gowan E. The intermediary cell: minor-vein anatomy and raffinose oligosaccharide synthesis in the Scrophulariaceae. Planta. 1993;191:446–56.
Turgeon R, Gowan E. Phloem loading in Coleus blumei in the absence of carrier-mediated uptake of export sugar from the apoplast. Plant Physiol. 1990;94:1244–9.
Turgeon R, Hepler PK. Symplastic continuity between mesophyll and companion cells in minor veins of mature Cucurbita pepo L. leaves. Planta. 1989;179:24–31.
Turgeon R, Medville R, Nixon KC. The evolution of minor vein phloem and phloem loading. Am J Bot. 2001;88:1331–9.
Turgeon R, Webb JA, Evert R. F. Ultrastructure of minor veins in Cucurbita pepo leaves. Protoplasma. 1975;83:217–32.
van Bel AJ. Sieve-pore plugging mechanisms. In: Baluska F, Volkman D, Barlow P, editors. Cell-cell channels. Boston: Landes Bioscience and Springer Science+Buisness Media; 2006. p. 113–8.
van Bel AJE. Strategies of phloem loading. Annu Rev Plant Physiol Plant Mol Biol. 1993;44:253–81.
Voitsekhovskaja OV, Koroleva OA, Batashev DR, Knop C, Tomos AD, Gamalei YV, et al. Phloem loading in two Scrophulariaceae species. What can drive symplastic flow via plasmodesmata? Plant Physiol. 2006;140:383–95.
Walker T. The purification and some properties of a protein causing gelling in phloem sieve tube exudate from Cucurbita pepo. Biochim Biophys Acta Protein Struct. 1972;257:433–44.
Walz C, Giavalisco P, Schad M, Juenger M, Klose J, Kehr J. Proteomics of curcurbit phloem exudate reveals a network of defence proteins. Phytochemistry. 2004;65:1795–804.
Webb J, Gorham P. Translocation of photosynthetically assimilated C14 in straight-necked squash. Plant Physiol. 1964;39:663.
Will T, van Bel AJ. Physical and chemical interactions between aphids and plants. J Exp Bot. 2006;57:729–37.
Williamson R. An investigation of the contractile protein hypothesis of phloem translocation. Planta. 1972;106:149–57.
Yadav UP, Ayre BG, Bush DR. Transgenic approaches to altering carbon and nitrogen partitioning in whole plants: assessing the potential to improve crop yields and nutritional quality. Front Plant Sci. 2015;6.
Zhang B, Tolstikov V, Turnbull C, Hicks LM, Fiehn O. Divergent metabolome and proteome suggest functional independence of dual phloem transport systems in cucurbits. Proc Natl Acad Sci U S A. 2010;107:13532–7.
Zhang C, Yu X, Ayre BG, Turgeon R. The origin and composition of cucurbit “phloem” exudate. Plant Physiol. 2012;158:1873–82.
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This work was supported by the National Science Foundation-Integrative Organismal Systems (1354718).
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Turgeon, R. (2016). Phloem Biology of the Cucurbitaceae. In: Grumet, R., Katzir, N., Garcia-Mas, J. (eds) Genetics and Genomics of Cucurbitaceae. Plant Genetics and Genomics: Crops and Models, vol 20. Springer, Cham. https://doi.org/10.1007/7397_2016_23
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