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RNAs and proteins localised in companion cell and sieve elements

Table 2. Examples of RNAs and proteins localized in the companion cell and/or sieve elements 

This table is a full version of the table (Table 2) that was generated for the review article submitted eLS with the title “Companion Cell and Sieve Elements” (Table 2., Kim and Frommer). Please feel free to contact us () if you would like to add any information to the list. At, Arabidopsis thaliana; Cm, Cucurbita maxima; Zm., Zea mays; St, Solanum tuberosum; Le, Lycopersicon esculentum; Mu, Mulberry.



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. doi.org/10.1242/dev.01231

Araya, T., Miyamoto, M., Wibowo, J., Suzuki, A., Kojima, S., Tsuchiya, Y.N., Sawa, S., Fukuda, H., von Wirén, N., Takahashi, H., 2014. CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proc. Natl. Acad. Sci. U.S.A. 111, 2029–2034. doi.org/10.1073/pnas.1319953111

Baker, R.F., Leach, K.A., Boyer, N.R., Swyers, M.J., Benitez-Alfonso, Y., Skopelitis, T., Luo, A., Sylvester, A., Jackson, D., Braun, D.M., 2016. Sucrose transporter ZmSut1 expression and localization uncover new insights into sucrose phloem loading. Plant Physiol. 172, 1876–1898. doi.org/10.1104/pp.16.00884

Barker, L., Kühn, C., Weise, A., Schulz, A., Gebhardt, C., Hirner, B., Hellmann, H., Schulze, W., Ward, J.M., Frommer, W.B., 2000. SUT2, a putative sucrose sensor in sieve elements. The Plant Cell 12, 1153–64.

Barrieu, F., Chaumont, F., Chrispeels, M.J., 1998. High expression of the tonoplast aquaporin ZmTIP1 in epidermal and conducting tissues of maize. Plant physiology 117, 1153–63.

Bezrutczyk, M., Zöllner, N.R., Kruse, C.P.S., Hartwig, T., Lautwein, T., Köhrer, K., Frommer, W.B., Kim, J.-Y., 2021. Evidence for phloem loading via the abaxial bundle sheath cells in maize leaves. Plant Cell 33, 531–547. doi.org/10.1093/plcell/koaa055

Bonke, M., Thitamadee, S., Mähönen, A.P., Hauser, M.-T., Helariutta, Y., 2003. APL regulates vascular tissue identity in Arabidopsis. Nature 426, 181–186. doi.org/10.1038/nature02100

Bostwick, D.E., Dannenhoffer, J.M., Skaggs, M.I., Lister, R.M., Larkins, B.A., Thompson, G.A., 1992. Pumpkin phloem lectin genes are specifically expressed in companion cells. Plant Cell 4, 1539–1548. doi.org/10.1105/tpc.4.12.1539

Clark, A.M., Jacobsen, K.R., Bostwick, D.E., Dannenhoffer, J.M., Skaggs, M.I., Thompson, G.A., 1997. Molecular characterization of a phloem-specific gene encoding the filament protein, phloem protein 1 (PP1), from Cucurbita maxima. The Plant Journal 12, 49–61.

Collum, T.D., Padmanabhan, M.S., Hsieh, Y.-C., Culver, J.N., 2016. Tobacco mosaic virus-directed reprogramming of auxin/indole acetic acid protein transcriptional responses enhances virus phloem loading. Proc. Natl. Acad. Sci. U.S.A. 113. doi.org/10.1073/pnas.1524390113

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. doi.org/10.1126/science.1141752

DeWitt, N.D., Harper, J.F., Sussman, M.R., 1991. Evidence for a plasma membrane proton pump in phloem cells of higher plants. The Plant Journal 1, 121–8.

DeWitt, N.D., Sussman, M.R., 1995. Immunocytological localization of an epitope-tagged plasma membrane proton pump (H(+)-ATPase) in phloem companion cells. Plant Cell 7, 2053–2067. doi.org/10.1105/tpc.7.12.2053

Fornara, F., Panigrahi, K.C.S., Gissot, L., Sauerbrunn, N., Rühl, M., Jarillo, J.A., Coupland, G., 2009. Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Developmental Cell 17, 75–86. doi.org/10.1016/j.devcel.2009.06.015

Fraysse, L.C., Wells, B., McCann, M.C., Kjellbom, P., 2005. Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells. Biology of the Cell 97, 519–534. doi.org/10.1042/BC20040122

Furuta, K.M., Hellmann, E., Helariutta, Y., 2014. Molecular control of cell specification and cell differentiation during procambial development. Annu. Rev. Plant Biol. 65, 607–638. doi.org/10.1146/annurev-arplant-050213-040306

Gai, Y.-P., Yuan, S.-S., Liu, Z.-Y., Zhao, H.-N., Liu, Q., Qin, R.-L., Fang, L.-J., Ji, X.-L., 2018. Integrated phloem sap mRNA and protein expression analysis reveals phytoplasma-infection responses in mulberry. Molecular & Cellular Proteomics 17, 1702–1719. doi.org/10.1074/mcp.RA118.000670

Hackel, A., Schauer, N., Carrari, F., Fernie, A.R., Grimm, B., Kuhn, C., 2006. Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. Plant J 45, 180–92. doi.org/10.1111/j.1365-313X.2005.02572.x

Haritatos, E., Ayre, B.G., Turgeon, R., 2000. Identification of phloem involved in assimilate loading in leaves by the activity of the galactinol synthase promoter. Plant Physiology 123, 929–937.

Hipper, C., Brault, V., Ziegler-Graff, V., Revers, F., 2013. Viral and cellular factors involved in phloem transport of plant viruses. Front. Plant Sci. 4. doi.org/10.3389/fpls.2013.00154

Ishiwatari, Y., Fujiwara, T., McFarland, K.C., Nemoto, K., Hayashi, H., Chino, M., Lucas, W.J., 1998. Rice phloem thioredoxin h has the capacity to mediate its own cell-to-cell transport through plasmodesmata. Planta 205, 12–22.

Khan, J.A., Wang, Q., Sjölund, R.D., Schulz, A., Thompson, G.A., 2007. An Early Nodulin-Like Protein accumulates in the sieve element plasma membrane of Arabidopsis. Plant Physiol. 143, 1576–1589. doi.org/10.1104/pp.106.092296

Kim, J.-Y., Symeonidi, E., Pang, T.Y., Denyer, T., Weidauer, D., Bezrutczyk, M., Miras, M., Zöllner, N., Hartwig, T., Wudick, M.M., Lercher, M., Chen, L.-Q., Timmermans, M.C.P., Frommer, W.B., 2021. Distinct identities of leaf phloem cells revealed by single cell transcriptomics. Plant Cell 33, 511–530. doi.org/10.1093/plcell/koaa060

Kühn, C., Franceschi, V.R., Schulz, A., Lemoine, R., Frommer, W.B., 1997. Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275, 1298–300.

Lucas, W.J., 1999. Plasmodesmata and the cell-to-cell transport of proteins and nucleoprotein complexes. J Exp Bot 50, 979–987.

Nakamura, S., Hayashi, H., Chino, M., 2006. Detection of calmodulin and calmodulin-binding proteins in pure phloem sap of rice plants. Soil Science and Plant Nutrition 52, 195–202. doi.org/10.1111/j.1747-0765.2006.00020.x

Ruiz-Medrano, R., Xoconostle-Cázares, B., Lucas, W.J., 1999. Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development 126, 4405–19.

Sanden, N.C., Schulz, A., 2022. Identification of new proteins in mature sieve elements. Physiologia Plantarum 174. doi.org/10.1111/ppl.13634

Schäffner, A.R., 1998. Aquaporin function, structure, and expression: are there more surprises to surface in water relations? Planta 204, 131–9.

Slewinski, T.L., Meeley, R., Braun, D.M., 2009. Sucrose transporter1 functions in phloem loading in maize leaves. J Exp Bot 60, 881–892. doi.org/10.1093/jxb/ern335

Truernit, E., Sauer, N., 1995. The promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene directs expression of β-glucuronidase to the phloem: Evidence for phloem loading and unloading by SUC2. Planta 196, 564–570. doi.org/10.1007/BF00203657

Ueki, S., Citovsky, V., 2002. The systemic movement of a tobamovirus is inhibited by a cadmium-ion-induced glycine-rich protein. Nat Cell Biol 4, 478–486. doi.org/10.1038/ncb806

Weise, A., Barker, L., Kühn, C., Lalonde, S., Buschmann, H., Frommer, W.B., Ward, J.M., 2000. A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate sieve elements of plants. Plant Cell 12, 1345–55.

Yoshimoto, N., Inoue, E., Saito, K., Yamaya, T., Takahashi, H., 2003. Phloem-Localizing Sulfate Transporter, Sultr1;3, Mediates Re-Distribution of Sulfur from Source to Sink Organs in Arabidopsis. Plant Physiology 131, 1511–1517. doi.org/10.1104/pp.014712

You, Y., Sawikowska, A., Lee, J.E., Benstein, R.M., Neumann, M., Krajewski, P., Schmid, M., 2019. Phloem companion cell-specific transcriptomic and epigenomic analyses identify MRF1, a regulator of flowering. Plant Cell 31, 325–345. doi.org/10.1105/tpc.17.00714

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