Abstract
XSP25, previously shown to be the most abundant hydrophilic protein in xylem sap of Populus nigra in winter, belongs to a secretory protein family in which the arrangement of basic and acidic amino acids is conserved between dicotyledonous and monocotyledonous species. Its gene expression was observed at the same level in roots and shoots under long-day conditions, but highly induced under short-day conditions and at low temperatures in roots, especially in endodermis and xylem parenchyma in the root hair region of Populus trichocarpa, and its protein level was high in dormant buds, but not in roots or branches. Addition of recombinant PtXSP25 protein mitigated the denaturation of lactate dehydrogenase by drying, but showed only a slight effect on that caused by freeze–thaw cycling. Recombinant PtXSP25 protein also showed ice recrystallization inhibition activity to reduce the size of ice crystals, but had no antifreezing activity. We suggest that PtXSP25 protein produced in shoots and/or in roots under short-day conditions and at non-freezing low temperatures followed by translocation via xylem sap to shoot apoplast may protect the integrity of the plasma membrane and cell wall functions from freezing and drying damage in winter environmental conditions.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- AFP:
-
Antifreeze protein
- BSA:
-
Bovine serum albumin
- BSP:
-
Basic secretory protein
- GLP:
-
Germin-like protein
- IRI:
-
Ice recrystallization inhibition
- LD:
-
Long-day
- LDH:
-
Lactate dehydrogenase
- LT:
-
Non-freezing low temperature
- qRT-PCR:
-
Real-time quantitative reverse-transcription polymerase chain reaction
- SD:
-
Short-day
- SDS:
-
Sodium dodecyl sulfate
- XSP:
-
Xylem sap protein
References
Aohara T, Mizuno H, Kiyomichi D, Abe Y, Matsuki K, Sagawa K, Mori H, Iwai H, Furukawa J, Satoh S (2016) Identification of a xylem sap germin-like protein and its expression under short-day and non-freezing low-temperature conditions in poplar root. Plant Biotechnol 33:123–127
Capicciotti CJ, Doshi M, Ben RN (2013) Ice recrystallization inhibitors: from biological antifreezes to small molecules. In: Wilson P (ed) Recent developments in the study of recrystallization. InTech, New York, pp 177–224
Capicciotti CJ, Kurach JDR, Turner TR, Mancini RS, Acker JP, Ben RN (2015) Small molecule ice recrystallization inhibitors enable freezing of human red blood cells with reduced glycerol concentrations. Sci Rep 5:9692
Chow-Shi-Yée M, Briard JG, Grondin M, Averill-Bates DA, Ben RN, Ouellet F (2016) Inhibition of ice recrystallization and cryoprotective activity of wheat proteins in liver and pancreatic cells. Protein Sci 25:974–986
Davies PL (2014) Ice-binding proteins: a remarkable diversity of structures for stopping and starting ice growth. Trends Biochem Sci 39:548–555
Dunwell JM, Gibbings JG, Mahmood T, Naqvi SMS (2008) Germin and germin-like proteins: evolution, structure, and function. Crit Rev Plant Sci 27:342–375
Emanuelsson O, Brunak S, Heijne GV, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP, and related tools. Nat Protoc 2:953–971
Eniade A, Purushotham M, Ben RN, Wang JB, Horwath W (2003) A serendipitous discovery of antifreeze protein-specific activity in C-linked antifreeze glycoprotein analogs. Cell Biochem Biophys 38:115–124
Furukawa J, Abe Y, Mizuno H, Matsuki K, Sagawa K, Kojima M, Sakakibara H, Iwai H, Satoh S (2011a) Seasonal fluctuation of organic and inorganic components in xylem sap of Populus nigra. Plant Root 5:56–62
Furukawa J, Abe Y, Mizuno H, Matsuki K, Sagawa K, Mori H, Iwai H, Satoh S (2011b) Abscisic acid-inducible 25 kDa xylem sap protein abundant in winter poplar. Plant Root 5:63–68
Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157
Houde M, Daniel C, Lachapelle M, Allard F, Laliberté S, Sarhan F (1995) Immunolocalization of freezing-tolerance-associated proteins in the cytoplasm and nucleoplasm of wheat crown tissues. Plant J 8:583–593
Ishikawa M, Sakai A (1982) Characteristics of freezing avoidance in comparison with freezing tolerance: a demonstration of extraorgan freezing. In: Li PH, Sakai A (eds) Plant cold hardiness and freezing stress, vol 2. Academic Press, New York, pp 325–340
Jang JY, Kim DG, Kim YO, Kim JS, Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 54:713–725
Jasik J, Schiebold S, Rolletschek H, Denolf P, Van Adenhove K, Altmann T, Borisjuk L (2011) Subtissue-specific evaluation of promoter efficiency by quantitative fluorometric assay in laser microdissected tissues of rapeseed. Plant Physiol 157:563–573
Karlson DT, Zeng Y, Stirm VE, Joly RJ, Ashworth EN (2003) Photoperiodic regulation of a 24-kD dehydrin-like protein in red-osier dogwood (Cornus sericea L.) in relation to freeze-tolerance. Plant Cell Physiol 44:25–34
Knight CA, Wen D, Laursen RA (1995) Nonequilibrium antifreeze peptides and the recrystallization of ice. Cryobiology 32:23–34
Kuwabara C, Arakawa K, Yoshida S (1999) Abscisic acid-induced secretory proteins in suspension-cultured cells of winter wheat. Plant Cell Physiol 40:184–191
Larcher W (2001a) Ökophysiologie der Pflanzen, 6th edn. Verlag Eugen Ulmer, Stuttgart, pp 301–312
Larcher W (2001b) Ökophysiologie der Pflanzen, 6th edn. Verlag Eugen Ulmer, Stuttgart, pp 322–323
Nilsson O, Alden T, Sitbon F, Little CHA, Chalupa V, Sandberg G, Olsson O (1992) Spatial pattern of cauliflower mosaic virus 35S promoter-luciferase expression in transgenic hybrid aspen trees monitored by enzymatic assay and non-destructive imaging. Transgenic Res 1:209–220
Nishimiya Y, Sato R, Takamichi M, Miura A, Tsuda S (2005) Co-operative effect of the isoforms of type III antifreeze protein expressed in Notched-fin eelpout, Zoarces elongatus Kner. FEBS J 272:482–492
Oda A, Sakuta C, Masuda S, Mizoguchi T, Kamada H, Satoh S (2003) Possible involvement of leaf gibberellins in the clock-controlled expression of XSP30, a gene encoding a xylem sap lectin, in cucumber roots. Plant Physiol 133:1779–1790
Ohtani M, Nishikubo N, Xu B, Yamaguchi M, Mitsuda N, Shi NGF, Ohme-Takagi M, Demura T (2011) A NAC domain protein family contributing to the regulation of wood formation in poplar. Plant J 67:499–512
Okushima Y, Koizumi N, Kusano T, Sano H (2000) Secreted proteins of tobacco cultured BY2 cells: identification of a new member of pathogenesis-related proteins. Plant Mol Biol 42:479–488
Sakuta C, Satoh S (2000) Vascular tissue-specific gene expression of xylem sap glycine-rich proteins in root and their localization in the walls of metaxylem vessels in cucumber. Plant Cell Physiol 41:627–638
Satoh S (2006) Organic substances in xylem sap delivered to above-ground organs by the roots. J Plant Res 119:179–187
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599
Tremblay K, Ouellet F, Fournier J, Danyluk J, Sarhan F (2005) Molecular characterization and origin of novel bipartite cold-regulated ice recrystallization inhibition proteins from cereals. Plant Cell Physiol 46:884–891
Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y (2006) Responses of the plasma membrane to low temperatures. Physiol Plant 126:81–89
Wan X, Zwiazek JJ, Lieffers VJ, Landhäusser SM (2001) Hydraulic conductance in aspen (Populus tremuloides) seedlings exposed to low root temperatures. Tree Physiol 21:691–696
Welling A, Palva ET (2006) Molecular control of cold acclimation in trees. Physiol Plant 127:167–181
Welling A, Moritz T, Palva ET, Junttila O (2002) Independent activation of cold acclimation by low temperature and short photoperiod in hybrid aspen. Plant Physiol 129:1633–1641
Wilson PW, Leader JP (1995) Stabilization of supercooled fluids by thermal hysteresis proteins. Biophys J 68:2098–2107
Wilson PW, Heneghan AF, Haymet ADJ (2003) Ice nucleation in nature: supercooling point measurement and the role of heterogeneous nucleation. Cryobiology 46:88–98
Wilson PW, Osterday KE, Heneghan AF, Haymet ADJ (2010) Effects of type 1 antifreeze proteins on the heterogeneous nucleation of aqueous solutions. J Biol Chem 285:34741–34745
Yamazaki T, Kawamura Y, Uemura M (2009) Extracellular freezing-induced mechanical stress and surface area regulation on the plasma membrane in cold-acclimated plant cells. Plant Signal Behav 4:231–233
Acknowledgements
We thank Drs. Misato Ohtani and Taku Demura of the Nara Institute of Science and Technology for their help regarding aseptic culture and genetic transformation of poplar. This work was supported in part by a Grant-in-Aid for Scientific Research (B) and for Scientific Research on Innovative Areas (24114006) to S.S.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Aohara, T., Furukawa, J., Miura, K. et al. Presence of a basic secretory protein in xylem sap and shoots of poplar in winter and its physicochemical activities against winter environmental conditions. J Plant Res 132, 655–665 (2019). https://doi.org/10.1007/s10265-019-01123-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-019-01123-9