Biologia plantarum 2019, 63:425-431 | DOI: 10.32615/bp.2019.061

Transcriptome profiling in Salix matsudana during refilling xylem vessels after embolism

Y.C. Yu, J.X. Liu*, Z.Y. Sun*
Research Institute of Forestry, State Key Laboratory of Tree Genetics and Breeding, and Key Laboratory of Tree Breeding and Cultivation of the State Forestry Administration, Chinese Academy of Forestry, Beijing 100091, P.R. China

The objective of this study is to understand the role of bark water uptake in refilling of xylem vessels after embolism in Salix matsudana. Further, we determined expression of genes closely related to xylem embolism repair. The isolated branch segments of S. matsudana were soaked in deionized water and after 2 h, the micro-computed tomography (CT) images, volume of xylem sap, osmotic potential of xylem sap, and the content of starch and soluble sugar were measured. At the same time, Illumina high-throughput sequencing (Hi Seq TM) was applied to obtain the xylem transcriptome profiling. The results showed that the soaked branches had 58.86 % fewer embolized vessels than branches before soaking. The volume of xylem sap was increased by 21.51 % in comparison with initial sample and the osmotic potential (Ψs) of xylem sap was decreased by 87.18 %. The content of ions and soluble sugars in the xylem sap significantly increased after soaking. Fourteen genes were clarified and found to have a significant correlation with osmotic potential of xylem sap. Our findings showed that water can enter the xylem vessels through the bark and can repair the xylem embolism in branches. The saccharides played an important role in osmotic potential difference formation and the genes UXL1 (uridine diphosphate-xylose synthase 1), UGDH (uridine diphosphate-glucose 6-dehydrogenase), BGLU40 (β-glucosidase 40), PPE8B (pectinesterase/pectinesterase inhibitor), UG1 (uridine diphosphate-glucuronate 1), and XYL4 (β-D-xylosidase 4)) were the key genes to promote embolized vessels refilling.

Keywords: bark water uptake, embolism repair, micro-computed tomography, osmotic potential, soluble sugars
Species: Salix matsudana

Received: March 7, 2018; Revised: August 8, 2018; Accepted: August 9, 2018; Prepublished online: March 22, 2019; Published: January 19, 2019Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Yu, Y.C., Liu, J.X., & Sun, Z.Y. (2019). Transcriptome profiling in Salix matsudana during refilling xylem vessels after embolism. Biologia plantarum63(1), 425-431. doi: 10.32615/bp.2019.061.
Download citation

Supplementary files

Download fileYU5695Suppl.pdf

File size: 1.34 MB

References

  1. Ameglio, T., Decourteix, M., Alves, G., Valentin, V., Sakr, S., Julien, J.L., Petel, G., Guilliot, A., Lacointe, A.: Temperature effects on xylem sap osmolarity in walnut trees: evidence for a vitalistic model of winter embolism repair. - Tree Physiol. 24: 785-793, 2001.
  2. Brodersen, C.R., McElrone, A.J., Choat, B., Lee, F., Shackel, K., Matthews, M.: In vivo visualizations of drought-induced embolism spread in Vitis vinifera. - Plant Physiol. 161:1820-1829, 2013.
  3. Bucci, S.J., Scholz, F.G., Goldstein, G., Meinzer, F.C., Sternberg, L.: Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the refilling of embolized vessels. - Plant Cell Environ. 26: 1633-1645, 2003. Go to original source...
  4. Christman, M.A., Sperry, J.S., Smith, D.D.: Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species. - New Phytol. 193: 713-720, 2012. Go to original source...
  5. Craig, R., Andrew, J., McElrone, A.: The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography. - Plant Physiol. 154: 1088-1095, 2010.
  6. Earles, M., Lucas, C.R., McElrone, A., Brodersen, C.: Bark water uptake promotes localized hydraulic recovery in coastal redwood crown. - Plant Cell Environ. 37: 617-626, 2015.
  7. Hacke, U.G., Sperry, J.S.: Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo. - Plant Cell Environ. 26: 303-311, 2003. Go to original source...
  8. Holtta, T., Vesala, T., Peramaki, M., Nikinmaa, E.: Refilling of embolised vessels as a consequence of 'Munch water' circulation. - Funct. Plant Biol. 33: 949-959, 2006. Go to original source...
  9. Laur, J., Hacke, U.G.: Transpirational demand affects aquaporin expression in poplar roots. - J. exp. Bot. 64: 2283-2293, 2013. Go to original source...
  10. Limm, E.B., Simonin, K.A., Bothman, A.G., Dawson, T.E.: Foliar water uptake: a common water acquisition strategy for plants of the redwood forest. - Oecologia 161: 449-459, 2009. Go to original source...
  11. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. - Methods 25: 402-408, 2001. Go to original source...
  12. Martorell, S., Diaz-Espejo, A., Medrano, H., Ball, M.C., Choat, B.: Rapid hydraulic recovery in Eucalyptus pauciflora after drought: linkages between stem hydraulics and leaf gas exchange. - Plant Cell Environ. 37: 617-626, 2014. Go to original source...
  13. Maurel, C., Verdoucq, L., Luu, D.T., Santoni, V.: Plant aquaporins: membrane channels with multiple integrated functions. - Annu. Rev. Plant Biol. 59: 595-624, 2008. Go to original source...
  14. Mayr, S., Schmid, P., Laur, J., Rosner, S., Charra Vaskou, K., Daemon, B., Hacke, U.: Uptake of water via branches helps timberline conifers refill embolized xylem in late winter. - Plant Physiol. 164: 1731-1740, 2014. Go to original source...
  15. Mayr, S., Wolfschwenger, M., Bauer, H.: Winter-drought induced embolism in Norway spruce (Picea abies) at the Alpine timberline. - Physiol. Plant. 115: 74-80, 2002. Go to original source...
  16. McCulloh, K., Sperry, J.S., Lachenbruch, B., Meinzer, F.C., Reich, P.B.: Moving water well: comparing hydraulic efficiency in twigs and trunks of coniferous, ring-porous, and diffuse-porous saplings from temperate and tropical forests. - New Phytol. 186: 439-450, 2010. Go to original source...
  17. Meinzer, F.C., Mc Culloh, K.A.: Xylem recovery from drought-induced embolism: where is the hydraulic point of no return? - Tree Physiol. 33: 331-334, 2013. Go to original source...
  18. Perrone, I., Pagliarani, C., Lovisolo, C., Chitarra, W., Roman, F., Schubert, A.: Recovery from water stress affects grape leaf petiole transcriptome. - Planta 235: 1383-1396, 2012. Go to original source...
  19. Salleo, S., Trifilo, P., Esposito, S., Nardini, A., Lo Gullo, M.A.: Starch-to-sugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair? - Funct. Plant Biol. 36: 815-825, 2009. Go to original source...
  20. Salleo, S., Trifilo, P., Gullo, M.A.L.: Phloem as a possible major determinant of rapid cavitation reversal in stems of Laurus nobilis (laurel). - Funct. Plant Biol. 33: 1063-1074, 2006. Go to original source...
  21. Secchi, F., Zwieniecki, M.A.: Patterns of PIP gene expression in Populus trichocarpa during recovery from xylem embolism suggest a major role for the PIP1 aquaporin subfamily as moderators of refilling process. - Plant Cell Environ. 33: 1285-1297, 2010. Go to original source...
  22. Secchi, F., Zwieniecki, M.A. Sensing embolism in xylem vessels: the role of sucrose as a trigger for refilling. - Plant Cell Environ. 34: 514-524, 2011. Go to original source...
  23. Secchi, F., Zwieniecki, M.A.: Down-regulation of plasma intrinsic protein1 aquaporin in poplar trees is detrimental to recovery from embolism. - Plant Physiol. 164: 1789-1799, 2014. Go to original source...
  24. Tyree, M.T., Salleo, S., Nardini, A., Lo Gullo, M.A., Mosca, R.: Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm? - Plant Physiol. 120: 11-21, 1999. Go to original source...
  25. Tyree, M.T., Zimmermann, M.H.: Xylem Structure and the Ascent of Sap. - Springer, Berlin 2002.
  26. Urli, M., Porte, A.J., Cochard, H., Guengant, Y., Burlett, R., Delzon, S.: Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. - Tree Physiol. 33: 672-683, 2013. Go to original source...
  27. Wang, C., Wang, L., Yang, C., Wang, Y.: Identification, phylogeny, and transcript profiling of aquaporin genes in response to abiotic stress in Tamarix hispida. - Tree Genet. Genomics 13: 81, 2017. Go to original source...
  28. Wheeler, J.K., Huggett, B.A., Tofte, A.N., Rockwell, F.E., Holbrook, N.M. Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. - Plant Cell Environ. 36: 1938-1949, 2013.
  29. Zwieniecki, M.A., Holbrook, N.M.: Confronting Maxwell's demon: biophysics of xylem embolism repair. - Trends Plant Sci. 14: 530-534, 2009. Go to original source...
  30. Zwieniecki, MA, Melcher, PJ, Ahrens, E.T.: Analysis of spatial and temporal dynamics of xylem refilling in Acer rubrum L. using magnetic resonance imaging. - Front. Plant Sci. 4: 265, 2013. Go to original source...