Phloem Long‐Distance Trafficking of Proteins and RNAs

Shmuel Wolf, The Hebrew University of Jerusalem, Rehovot, Israel

Published online: December 2009

DOI: 10.1002/9780470015902.a0021260

Phloem sap contains a wide range of macromolecules, including ribonucleic acids (RNAs) and proteins. Recent advances in genomic and proteomic technologies have enabled the identification of thousands of these macromolecules. However, technical limitations are still the main obstacle to the complete characterization of macromolecule profiles in the sieve tube.

Grafting experiments have established that numerous macromolecules are capable of moving long distances between tissues, providing the foundation for the hypothesis of an interorgan information superhighway in higher plants involving the phloem. This chapter presents the current knowledge on proteins and messenger RNA (mRNA) molecules present in the sieve tube. The challenge now is to characterize the biological role of trafficking macromolecules, such as their involvement in the signal-transduction pathway(s) elicited by environmental cues and in orchestrating developmental processes at the whole-plant level.

Key concepts

  • Phloem sap contains macromolecules such as proteins and RNAs.
  • Protein profiles in the sieve tube are tissue specific.
  • Phloem proteins act as long-distance signalling molecules.
  • Plant viruses move long distance via the phloem.
  • Endogenous RNA molecules are capable of trafficking long distance via the phloem.
  • mRNA molecules may act as long-distance signalling molecules.

Keywords: companion cell; heterograft; plasmodesmata; sieve element

Figure 1. Models for the two mechanisms of phloem loading of sugars into the sieve tube of higher plants. (a) Symplastic phloem loading. Sucrose is transported symplastically all the way from the mesophyll (MC) to intermediary cells (ICs), which are a special type of companion cells (CC). In the ICs, sucrose is converted to raffinose and stachyose which are then translocated long distances within the sieve tube. (b) Apoplastic phloem loading. Sucrose exits to the apoplast and then is actively loaded by sucrose transporters. Note that there are a small number of plasmodesmata (PD) interconnecting the bundle sheath (BS)/phloem parenchyma (PP) with CCs. It is assumed that these PD provide a route for the trafficking of information molecules. SE; sieve element and SAP, phloem sap collected from cut sieve tube.
Figure 2. A model for the ‘wave’ pattern long-distance movement of plant viruses. CC, companion cell and SE, sieve element. Virus particles are unloaded from the SEs to the CCs for replication, forming an additional ‘wave’ for further movement.
Figure 3. Functional classification of transcripts identified in phloem sap collected from melon stems: 1152 characterized ESTs (based on BLAST description) were classified into 10 categories. The percentage of ESTs assigned to each category is indicated.
close
 References
    Aoki K, Kragler F, Xoconostle-Cázares B and Lucas WJ (2002) A subclass of plant heat shock cognate 70 chaperones carries a motif that facilitates trafficking through plasmodesmata. Proceedings of the National Academy of Sciences of the USA 99: 16342–16347.
    Aoki K, Suzui N, Fujimaki S et al. (2005) Destination-selective long-distance movement of phloem proteins. Plant Cell 17: 1801–1814.
    Asano T, Masumura T, Kusano H et al. (2002) Construction of a specialized cDNA library from plant cells isolated by laser capture microdissection: toward comprehensive analysis of the genes expressed in the rice phloem. Plant Journal 32: 401–408.
    Balachandran S, Xiang Y, Schobert C, Thompson GA and Lucas WJ (1997) Phloem sap proteins from Cucurbita maxima and Ricinus communis have the capacity to traffic cell to cell through plasmodesmata. Proceedings of the National Academy of Sciences of the USA 94: 14150–14155.
    Banerjee AK, Chatterjee M, Yu Y et al. (2006) Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell 18: 3443–3457.
    Buhtz A, Springer F, Chappell L, Baulcombe DC and Kehr J (2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant Journal 53: 739–749.
    la Cour Petersen M, Hejgaard J, Thompson GA and Schulz A (2005) Cucurbit phloem serpins are graft-transmissible and appear to be resistant to turnover in the sieve element-companion cell complex. Journal of Experimental Botany 56: 3111–3120.
    Corbesier L, Vincent C, Jang S et al. (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316: 1030–1033.
    Germundsson A and Valkonen JPT (2006) P1- and VPg-transgenic plants show similar resistance to Potato virus A and may compromise long distance movement of the virus in plant sections expressing RNA silencing-based resistance. Virus Research 116: 208–213.
    Giakountis A and Coupland G (2008) Phloem transport of flowering signals. Current Opinion in Plant Biology 11: 687–694.
    Gómez G, Torres H and Pallás V (2005) Identification of translocatable RNA-binding phloem proteins from melon, potential components of the long-distance RNA transport system. Plant Journal 41: 107–116.
    Gosalvez-Bernal B, Genoves A, Navarro JA, Pallas V and Sanchez-Pina MA (2008) Distribution and pathway for phloem-dependent movement of Melon necrotic spot virus in melon plants. Molecular Plant Pathology 9: 447–461.
    Ham B-K, Brandon JL, Xoconostle-Cazares B et al. (2009) A polypyrimidine tract binding protein, pumpkin RBP50, forms the basis of a phloem-mobile ribonucleoprotein complex. Plant Cell 21: 197–215.
    Haywood V, Yu T-S, Huang N-C and Lucas WJ (2005) Phloem long-distance trafficking of GIBBERELLIC ACID-INSENSITIVE RNA regulates leaf development. Plant Journal 42: 49–68.
    Imlau A, Truernit E and Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11: 309–322.
    Jaeger KE and Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Current Biology 17: 1050–1054.
    Kehr J (2006) Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. Journal of Experimental Botany 57: 767–774.
    Kehr J and Buhtz A (2008) Long distance transport and movement of RNA through the phloem. Journal of Experimental Botany 59: 85–92.
    Kehr J, Haebel S, Blechschmidt-Schneider S et al. (1999) Analysis of phloem protein patterns from different organs of Cucurbita maxima Duch. By matrix-assisted laser desorption/ionization time of flight mass spectroscopy combined with sodium dodecyl sulfate polyacrylamide gel electrophoresis. Planta 207: 612–619.
    Kim M, Canio W, Kessler S and Sinha N (2001) Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293: 287–289.
    Lin M-K, Belanger H, Lee Y-J et al. (2007) FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell 19: 1488–1506.
    Moreno IM, Thompson JR and García-Arenal F (2004) Analysis of the systemic colonization of cucumber plants by Cucumber green mottle mosaic virus. Journal of General Virology 85: 749–759.
    Nakazono M, Qiu F, Borsuk LA and Schnable PS (2003) Laser capture microdissection, a tool for the global analysis of gene expression in specific cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell 15: 583–596.
    Omid A, Keilin T, Glass D, Leshkowitz D and Wolf S (2007) Characterization of phloem-sap transcription profile in melon plants. Journal of Experimental Botany 58: 3645–3656.
    Oparka KJ and Santa Cruz S (2000) The great escape: phloem transport and unloading of macromolecules. Annual Review of Plant Physiology and Plant Molecular Biology 51: 323–347.
    Oparka KJ and Turgeon R (1999) Sieve elements and companion cells: traffic control centers of the phloem. Plant Cell 11: 739–750.
    Palauqui J-C, Elmayan T, Pollien J-M and Vaucheret H (1997) Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO Journal 16: 4738–4745.
    Palukaitis P (1987) Potato spindle tuber viroid. Investigation of the long-distance, intra-plant transport route. Virology 158: 239–241.
    Peleg G, Malter D and Wolf S (2007) Viral infection enables phloem loading of GFP and long-distance trafficking of the protein. Plant Journal 51: 165–172.
    Ruiz-Medrano R, Xoconostle-Cázares B and Lucas WJ (1999) Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development 126: 4405–4419.
    Santa Cruz S (1999) Perspective: phloem transport of viruses and macromolecules – what goes in must come out. Trends in Microbiology 7: 237–241.
    Scholthof HB (2005) Plant virus transport: motions of functional equivalence. Trends in Plant Science 10: 376–382.
    Tamaki S, Matsuo S, Wong HL, Yokoi S and Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316: 1033–1036.
    Taoka K, Ham BK, Xoconostle-Cázares B, Rojas MR and Lucas WJ (2007) Reciprocal phosphorylation and glycosylation recognition motifs control NCAPP1 interaction with pumpkin phloem proteins and their cell-to-cell movement. Plant Cell 19: 1866–1884.
    Van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant Cell and Environment 26: 125–149.
    Vilaine F, Palauqui J-C, Amselem J et al. (2003) Towards deciphering phloem: a transcriptome analysis of the phloem of Apium graveolens. Plant Journal 36: 67–81.
    Walz C, Giavalisco P, Schad M et al. (2004) Proteomics of curcurbit phloem exudate reveals a network of defence proteins. Phytochemistry 65: 1795–1804.
    Wisniewski LA, Powell PA, Nelson RS and Beachy RN (1990) Local and systemic spread of tobacco mosaic virus in transgenic tobacco. Plant Cell 2: 559–567.
    Xoconostle-Cazares B, Yu X, Ruiz-Medrano R et al. (1999) Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science 283: 94–98.
    Yoo BC, Kragler F, Varkonyi-Gasic E et al. (2004) A systemic small RNA signaling system in plants. Plant Cell 16: 1979–2000.
    Zhong X, Tao X, Stombaugh J, Leontis N and Ding B (2007) Tertiary structure and function of an RNA motif required for plant vascular entry to initiate systemic trafficking. EMBO Journal 26: 3836–3846.
    Zhu Y, Green L, Woo YM, Owens R and Ding B (2001) Cellular basis of potato spindle tuber viroid systemic movement. Virology 279: 69–77.
 Further Reading
    Haywood V, Kragler F and Lucas WJ (2002) Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell 14: S303–S325.
    Lough TJ and Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annual Review of Plant Biology 57: 203–232.
    Thompson GA and Schulz A (1999) Macromolecular trafficking in the phloem. Trends in Plant Science 4: 354–360.
    Van Bel AJE (1993) Strategies of phloem loading. Annual Review of Plant Physiology and Plant Molecular Biology 44: 253–281.

Related Sub-Topics:

Viruses Infecting Plants | RNA Viruses | Plant Development | Plant Genetics and Molecular Biology | Plant Stress Physiology
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Phloem Long‐Distance Trafficking of Proteins and RNAs
 
How to Cite close
Wolf, Shmuel(Dec 2009) Phloem Long‐Distance Trafficking of Proteins and RNAs. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021260]