Abstract
Main conclusion
The work demonstrates a relationship between the biosynthesis of the secondary metabolite, agatharesinol, and cytological changes that occur in ray parenchyma during cell death in sapwood sticks of Cryptomeria japonica under humidity-regulated conditions.
To characterize the death of ray parenchyma cells that accompanies the biosynthesis of secondary metabolites, we examined cell death in sapwood sticks of Cryptomeria japonica under humidity-regulated conditions. We monitored features of ray parenchyma cells, such as viability, the morphology of nuclei and vacuoles, and the amount of starch grains. In addition, we analyzed levels of agatharesinol, a heartwood norlignan, by gas chromatography–mass spectrometry in the same sapwood sticks. Dramatic changes in the amount of starch grains and in the level of agatharesinol occurred simultaneously. Therefore, the biosynthesis of agatharesinol appeared to originate from the breakdown of starch. Furthermore, we observed the expansion of vacuoles in ray parenchyma cells prior to other cytological changes at the final stage of cell death. In our experimental system, we were able to follow the process of cell death and to demonstrate relationships between cytological changes and the biosynthesis of a secondary metabolite during the death of ray parenchyma cells.
Similar content being viewed by others
Abbreviations
- DAPI:
-
4′,6-Diamidino-2-phenylindole
- FDA:
-
Fluorescein diacetate
- GC–MS:
-
Gas chromatography–mass spectrometry
- I2/KI:
-
Iodine-potassium iodide
- NR:
-
Neutral red
- PBS:
-
Phosphate-buffered saline
- PI:
-
Propidium iodide
- TEM:
-
Transmission electron microscopy
References
Bamber RK, Fukazawa K (1985) Sapwood and heartwood: a review. For Abstract 46:567–580
Begum S, Nakaba S, Oribe Y, Kubo T, Funada R (2007) Induction of cambial reactivation by localized heating in a deciduous hardwood hybrid poplar (Populus sieboldii × P. grandidentata). Ann Bot 100:439–447
Begum S, Nakaba S, Oribe Y, Kubo T, Funada R (2010) Changes in the localization and levels of starch and lipids in cambium and phloem during cambial reactivation by artificial heating of main stems of Cryptomeria japonica trees. Ann Bot 106:885–895
Bito N, Nakada R, Fukatsu E, Matsushita Y, Fukushima K, Imai T (2011) Clonal variation in heartwood norlignans of Cryptomeria japonica: evidence for independent control of agatharesinol and sequirin C biosynthesis. Ann For Sci 68:1049–1056
Catesson AM (1990) Cambial cytology and biochemistry. In: Iqbal M (ed) The vascular cambium. Research Studies Press, Taunton, pp 63–112
Chaffey N, Barlow P (2001) The cytoskeleton facilitates a three-dimensional symplastic continuum in the long-lived ray and axial parenchyma cells of angiosperm trees. Planta 213:811–823
Dubrovsky JG, Guttenberger M, Saralegui A, Napsucialy-Mendivil S, Voigt B, Baluska F, Menzel D (2006) Neutral red as a probe for confocal laser scanning microscopy studies of plant roots. Ann Bot 97:1127–1138
Duchesne LC, Hubbes M, Jeng RS (1992) Biochemistry and molecular biology of defense reaction in the xylem of angiosperm trees. In: Blanchette RA, Biggs AR (eds) Defense mechanisms of woody plants against fungi. Springer, Berlin, pp 133–146
Ehara M, Noguchi T, Ueda K (1996) Uptake of neutral red by the vacuoles of a green alga, Micrasterias pinnatifida. Plant Cell Physiol 37:734–741
Fukuda H (2004) Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5:379–391
Hara-Nishimura I, Hatsugai N (2011) The role of vacuoles in plant cell death. Cell Death Differ 18:1298–1304
Hillis WE (1987) Heartwood and tree exudates. Springer, New York, pp 1–268
Höll W (2000) Distribution, fluctuation and metabolism of food reserves in the wood of trees. In: Savidge R, Barnett J, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers, Oxford, pp 347–362
Imai T, Nomura M (2005) Induction of the biosynthesis of agatharesinol, a norlignan, in sapwood sticks of Cryptomeria japonica under humidity-regulated circumstances. J Wood Sci 51:537–541
Imai T, Nomura M, Fukushima K (2006a) Evidence for involvement of the phenylpropanoid pathway in the biosynthesis of the norlignan agatharesinol. J Plant Physiol 163:483–487
Imai T, Nomura M, Matsushita Y, Fukushima K (2006b) Hinokiresinol is not a precursor of agatharesinol in the norlignan biosynthetic pathway in Japanese cedar. J Plant Physiol 163:1221–1228
Jones KH, Senft JA (1985) An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide. J Histochem Cytochem 33:77–79
Kariya K, Demiral T, Sasaki T, Tsuchiya Y, Turkan I, Sano T, Hasezawa S, Yamamoto Y (2013) A novel mechanism of aluminum-induced cell death involving vacuolar processing enzyme and vacuolar collapse in tobacco cell line BY-2. J Inorg Biochem 128:196–201
Kemp MS, Burden RS (1986) Phytoalexins and stress metabolites in the sapwood of trees. Phytochemistry 25:1261–1269
Kuriyama H, Fukuda H (2002) Developmental programmed cell death in plants. Curr Opin Plant Biol 5:568–573
Magel EA (2000) Biochemistry and physiology of heartwood formation. In: Savidge R, Barnett J, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers, Oxford, pp 363–376
Magel EA, Hillinger C, Höll W, Ziegler H (1997) Biochemistry and physiology of heartwood formation: role of reserve substances. In: Rennenberg H, Eschrich W, Ziegler H (eds) Trees—contributions to modern tree physiology. SFB Academic Publisher, The Hague, pp 477–506
Morel A, Teyssier C, Trontin JF, Eliášová K, Pešek B, Beaufour M, Morabito D, Boizot N, Le Metté C, Belal-Bessai L, Reymond I, Harvengt L, Cadene M, Corbineau F, Vágner M, Label P, Lelu-Walter MA (2014) Early molecular events involved in Pinus pinaster Ait. somatic embryo development under reduced water availability: transcriptomic and proteomic analyses. Physiol Plant 152:184–201
Murakami Y, Funada R, Sano Y, Ohtani J (1999) The differentiation of contact cells and isolation cells in the xylem ray parenchyma of Populus maximowiczii. Ann Bot 84:429–435
Nakaba S, Sano Y, Kubo T, Funada R (2006) The positional distribution of cell death of ray parenchyma in a conifer, Abies sachalinensis. Plant Cell Rep 25:1143–1148
Nakaba S, Kubo T, Funada R (2008a) Differences in patterns of cell death between ray parenchyma cells and ray tracheids in the conifers Pinus densiflora and Pinus rigida. Trees 22:623–630
Nakaba S, Yoshimoto J, Kubo T, Funada R (2008b) Morphological changes in the cytoskeleton, nuclei, and vacuoles during cell death of short-lived ray tracheids in the conifer Pinus densiflora. J Wood Sci 54:509–514
Nakaba S, Begum S, Yamagishi Y, Jin HO, Kubo T, Funada R (2012) Differences in the timing of cell death, differentiation and function among three different types of ray parenchyma cells in the hardwood Populus sieboldii × P. grandidentata. Trees 26:743–750
Nakaba S, Sano Y, Funada R (2013) Disappearance of microtubules, nuclei and starch during cell death of ray parenchyma in Abies sachalinensis. IAWA J 34:135–146
Nakaba S, Takata N, Yoshida M, Funada R (2015a) Continuous expression of genes for xylem cysteine peptidases in long-lived ray parenchyma cells in Populus. Plant Biotechnol 32:21–29
Nakaba S, Kitin P, Yamagishi Y, Begum S, Kudo K, Nugroho WD, Funada R (2015b) Three-dimensional imaging of cambium and secondary xylem cells by confocal laser scanning microscopy. In: Yeung ECT, Stasolla C, Sumner MJ, Huang BQ (eds) Plant microtechniques and protocols. Springer, Switzerland, pp 431–465
Nobuchi T, Harada H (1985) Ultrastructural changes in parenchyma cells of sugi (Cryptomeria japonica D. Don) associated with heartwood formation. Mokuzai Gakkaishi 31:965–973
Nobuchi T, Kuroda K, Iwata R, Harada H (1982) Cytological study of the seasonal features of heartwood formation of sugi (Cryptomeria japonica D. Don). Mokuzai Gakkaishi 28:669–676
Nobuchi T, Akamatsu Y, Sato K, Harada H (1986) Early response of ray parenchyma cells following wounding in sugi (Cryptomeria japonica D. Don) wood: seasonal changes of discoloration and cytological structure. Bull Kyoto Univ For 57:290–299
Ohashi H, Imai T (1990) Characterization of physiological functions of sapwood: synthesis and accumulation of heartwood extractives in the withering process of immature Japanese cedar trunk. Holzforschung 44:317–323
Ohashi H, Imai T, Yoshida K, Yasue M (1990) Characterization of physiological functions of sapwood: fluctuation of extractives in the withering process of Japanese cedar sapwood. Holzforschung 44:79–86
Ohashi H, Kato N, Imai T, Kawai S (1991) Characterization of physiological functions of sapwood: fluctuation of heartwood extractives in the withering process of Japanese cedar sapwood fed an inhibitor of phenylalanine ammonia-lyase. Holzforschung 45:245–252
Rasband WS (1997–2015) ImageJ. US National Institutes of Health, Bethesda. http://rsb.info.nih.gov/ij/
Rotman BB, Papermaster BW (1966) Membrane properties of living mammalian cells as studied by hydrolysis of fluorogenic esters. Proc Nat Acad Sci USA 55:134–141
Sauter JJ (2000) Photosynthate allocation to the vascular cambium: fact and problem. In: Savidge R, Barnett J, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers, Oxford, pp 71–83
Shigo AL (1984) Compartmentalization: a conceptual framework for understanding how trees grow and defend themselves. Annu Rev Phytopathol 22:189–214
Spicer R (2005) Senescence in secondary xylem: heartwood formation as an active developmental program. In: Holbrook NM, Zwieniecki MA (eds) Vascular transport in plants. Elsevier Academic Press, Amsterdam, pp 457–475
Spicer R (2014) Symplasmic networks in secondary vascular tissues: parenchyma distribution and activity supporting long-distance transport. J Exp Bot 65:1829–1848
Taylor A, Gartner BL, Morrell JJ (2002) Heartwood formation and natural durability—a review. Wood Fiber Sci 34:587–611
van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, Mur LA, Petersen M, Smertenko A, Taliansky M, van Breusegem F, Wolpert T, Woltering E, Zhivotovsky B, Bozhkov PV (2011) Morphological classification of plant cell deaths. Cell Death Differ 18:1241–1246
Yamada T (2001) Defense mechanisms in the sapwood of living trees against microbial infection. J For Res 6:127–137
Yanase Y, Sakamoto K, Imai T (2015) Isolation and structural elucidation of norlignan polymers from the heartwood of Cryptomeria japonica. Holzforschung 69:281–296
Yoshida K, Nishiguchi M, Hishiyama S, Kato A, Takahashi K (2006) Generation and alteration of norlignans in a transition zone during the drying of a Cryptomeria japonica log. J Wood Sci 52:372–375
Yoshida K, Nihiguchi M, Futamura N, Nanjo T (2007) Expressed sequence tags from Cryptomeria japonica sapwood during the drying process. Tree Physiol 27:1–9
Acknowledgments
The authors thank Mr. Shinichi Sato (Forestry and Forest Products Research Institute, Forest Tree Breeding Center) for help in the collection of samples. This work was supported by Grants-in-Aid from the Japan Society for the Promotion of Science (Nos. 23380105, 24380090, 25850121, 15H04527 and 15K07508).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Nakaba, S., Arakawa, I., Morimoto, H. et al. Agatharesinol biosynthesis-related changes of ray parenchyma in sapwood sticks of Cryptomeria japonica during cell death. Planta 243, 1225–1236 (2016). https://doi.org/10.1007/s00425-016-2473-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-016-2473-y