Abstract
Key message
Calli of hybrid poplar that had been exposed to desiccation in air before transfer to the induction medium differentiated into tracheary elements at higher rates than calli without air desiccation.
Abstract
Cells of hybrid poplar (Populus sieboldii x P. grandidentata) in culture can be induced to differentiate into secondary xylem-like tracheary elements that form the highly developed bordered pits and broad regions of cell walls in contrast to helical or reticulate wall thickenings in primary xylem elements. We attempted to increase the rate of differentiation of tracheary elements from calli using a combination of hormonal stimulation and partial desiccation. Calli that had been exposed to desiccation in air in a clean hood for 90 min before transfer to the induction medium differentiated into tracheary elements at higher rates than calli without air desiccation. The partial desiccation treatment had no effects on the features of the induced tracheary elements and the frequencies with which they appeared. Our results show that partial desiccation can increase, approximately threefold the rate of differentiation of secondary xylem-like tracheary elements from calli of hybrid poplar. This improvement in the rate of differentiation tracheary elements in vitro should facilitate detailed future analysis of the differentiation of secondary xylem.
References
Abe H, Funada R (2005) The orientation of cellulose microfibrils in the cell walls of tracheids in conifer: a model based on observations by field emission-scanning electron microscopy. IAWA J 26:161–174. doi:10.1163/22941932-90000108
Busov VB, Brunner AM, Meilan R, Filichkin S, Ganio L, Gandhi S, Strauss SH (2005) Genetic transformation: a powerful tool for dissection of adaptive traits in trees. New Phytol 167:9–18. doi:10.1111/j.1469-8137.2005.01412.x
Chasan R (1994) Tracing tracheary element development. Plant Cell 6:917–919. doi:10.1105/tpc.6.7.917
Devillard C, Walter C (2014) Formation of plant tracheary elements in vitro—a review. New Zeal J For Sci 44:22. doi:10.1186/s40490-014-0022-7
Franklin GL (1945) Preparation of thin sections of synthetic resins and wood-resin composites, and a new macerating method for wood. Nature 155:51. doi:10.1038/155051a0
Fukuda H (1997) Tracheary element differentiation. Plant Cell 9:1147–1156. doi:10.1105/tpc.9.7.1147
Fukuda H, Komamine A (1980) Establishment of an experimental system for the study of tracheary element differentiation from single cells isolated from the mesophyll of Zinnia elegans. Plant Physiol 65:57–60. doi:10.1104/pp.65.1.57
Funada R, Yamagishi Y, Begum S, Kudo K, Nabeshima E, Nugroho WD, Hasnat R, Oribe Y, Nakaba S (2016) Xylogenesis in trees: from cambial cell division to cell death. In: Kim YS, Funada R, Singh AP (eds) Secondary xylem biology. Academic Press, Elsevier, Amsterdam, pp 25–43
Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458. doi:10.1146/annurev.arplant.58.032806.103956
Kaur A, Gosal SS (2009) Desiccation of callus enhances somatic embryogenesis and subsequent shoot regeneration in sugarcane. Indian J Biotechnol 8:332–334
Kermode AR, Dumbroff EB, Bewley JD (1989) The role of maturation drying in the transition from seed development to germination. J Exp Bot 40:303–313. doi:10.1093/jxb/40.2.303
King RW (1976) Abscisic acid in developing wheat grains and its relationship to grain growth and maturation. Planta 132:43–51. doi:10.1007/BF00390329
Kitin P, Funada R, Sano Y, Beeckman H, Ohtani J (1999) Variations in the lengths of fusiform cambial cells and vessel elements in Kalopanax pictus. Ann Bot 84:621–632. doi:10.1006/anbo.1999.0957
Malabadi R, Choudhury H, Tandon P (2004) Initiation, maintenance and maturation of somatic embryos from thin apical dome section in Pinus kesiya (Royle ex. Gord) promoted by partial desiccation and gellan gum. Sci Hortic 102:449–459. doi:10.1016/j.scienta.2004.06.001
Motose H, Fukuda H, Sugiyama M (2001) Involvement of local intercellular communication in the differentiation of Zinnia mesophyll cells into tracheary elements. Planta 213:121–131. doi:10.1007/s004250000482
Motose H, Sugiyama M, Fukuda H (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429:873–878. doi:10.1038/nature02613
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. doi:10.1111/j.1399-3054.1962.tb08052.x
Oda Y, Mimura T, Hasezawa S (2005) Regulation of secondary cell wall development by cortical microtubules during tracheary element differentiation in Arabidopsis cell suspensions. Plant Physiol 137:1027–1036. doi:10.1104/pp.104.052613
Oda Y, Iida Y, Kondo Y, Fukuda H (2010) Wood cell-wall structure requires local 2D-microtubule disassembly by a novel plasma membrane-anchored protein. Curr Biol 20:1197–1202. doi:10.1016/j.cub.2010.05.038
Othmani A, Bayoudh C, Drira N, Marrakchi M, Trifi M (2009) Somatic embryogenesis and plant regeneration in date palm Phoenix dactylifera L., cv. Boufeggous is significantly improved by fine chopping and partial desiccation of embryogenic callus. Plant Cell Tiss Organ Cult 97:71–79. doi:10.1007/s11240-009-9500-7
Pesquet E, Korolev AV, Calder G, Lloyd CW (2010) The microtubule-associated protein AtMAP70-5 regulates secondary wall patterning in Arabidopsis wood cells. Curr Biol 20:744–749. doi:10.1016/j.cub.2010.02.057
Rancé IM, Tian W, Mathews H, de Kochko A, Beachy RN, Fauquet C (1994) Partial desiccation of mature embryo-derived calli, a simple treatment that dramatically enhances the regeneration ability of indica rice. Plant Cell Rep 13:647–651. doi:10.1007/BF00232938
Roberts DR, Lazaroff WR, Webster FB (1991) Interaction between maturation and high relative humidity treatments and their effects on germination of sitka spruce somatic embryos. J Plant Physiol 138:1–6. doi:10.1016/S0176-1617(11)80720-0
Sterky F, Regan S, Karlsson J, Hertzberg M, Rohde A, Holmberg A, Amini B, Bhalerao R, Larsson M, Villarroel R, Van Montagu M, Sandberg G, Olsson O, Teeri TT, Boerjan W, Gustafsson P, Uhle´n M, Sundberg B, Lundeberg J (1998) Gene discovery in the wood-forming tissues of poplar: analysis of 5692 expressed sequence tags. Proc Natl Acad Sci USA 95:13330–13335. doi:10.1073/pnas.95.22.13330
Sterky F, Bhalerao RR, Unneberg P, Segerman B, Nilsson P, Brunner AM, Charbonnel-Campaa L, Lindvall JJ, Tandre K, Strauss SH, Sundberg B, Gustafsson P, Uhle´n M, Bhalerao RP, Nilsson O, Sandberg G, Karlsson J, Lundeberg J, Jansson S (2004) A Populus EST resource for plant functional genomics. Proc Natl Acad Sci USA 101:13951–13956. doi:10.1073/pnas.0401641101
Tuskan GA, Difazio S, Jansson S, Bohlmann J et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. and Gray). Science 313:1596–1604. doi:10.1126/science.1128691
Yamagishi Y, Sato T, Uchiyama H, Yoshimoto J, Nakagawa R, Nakaba S, Kubo T, Funada R (2012) Tracheary elements that resemble secondary xylem in calli derived from the conifers, Torreya nucifera and Cryptomeria japonica. J Wood Sci 58:557–562. doi:10.1007/s10086-012-1288-0
Yamagishi Y, Yoshimoto J, Uchiyama H, Nabeshima E, Nakaba S, Watanabe U, Funada R (2013) In vitro induction of secondary xylem-like tracheary elements in calli of hybrid poplar (Populus sieboldii x P. grandidentata). Planta 237:1179–1185. doi:10.1007/s00425-013-1839-7
Yamagishi Y, Uchiyama H, Sato T, Kitamura K, Yoshimoto J, Nakaba S, Watanabe U, Funada R (2015) In vitro induction of the formation of tracheary elements from suspension-cultured cells of the conifer Cryptomeria japonica. Trees 29:1283–1289. doi:10.1007/s00468-014-1139-2
Acknowledgments
This work was supported, in part, by Grants-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Culture of Japan (Nos. 20120009, 21380107, 24380090, 24 · 2976 and 15H04527) and by Scholarship and Education Funds from Nisshin Sugar Manufacturing Co., Ltd.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by H. Rennenberg.
Rights and permissions
About this article
Cite this article
Yamagishi, Y., Yoshimoto, J., Ide, S. et al. Partial desiccation enhances induction of secondary xylem-like tracheary elements from calli of hybrid poplar (Populus sieboldii x P. grandidentata). Trees 31, 1083–1089 (2017). https://doi.org/10.1007/s00468-016-1411-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-016-1411-8