ORIGINAL ARTICLELocally heated dormant cambium can re-initiate cell production independently of new shoot growth in deciduous conifers (Larix kaempferi)
Introduction
Trees accumulate the remains of cells derived from the meristem of vascular cambium, which are differentiated into secondary xylem (wood) or secondary phloem, in their stems under various environmental conditions. In the cool-temperate and temperate zones, the cambium in trees usually undergoes annual periods of cell production, namely cambial activity and winter cambial dormancy. Cambial cell division stops during the dormant period and resumes in early spring, thereby accounting for the formation of growth rings in trees. Cambial reactivation, which is the resumption of cell division in the dormant cambium, has long been one of the most significant subjects of cambium studies (see reviews of Priestley, 1930, Romberger, 1963, Savidge and Wareing, 1981a, Sundberg et al., 2000, Frankenstein et al., 2005, Prislan et al., 2013). This is one of the processes that controls earlywood width and annual ring width, thereby affecting wood quantity and quality, for example, density.
Many studies have aimed to elucidate the trigger of cambial reactivation (see reviews of Wareing, 1951, Romberger, 1963, Brown, 1971, Sundberg et al., 1991, Sundberg et al., 2000). Some of the new insights provided by these studies include: 1) an apparent temporal correlation between the re-initiation of cambial activity and spring bud flushing; 2) the initial commencement of cambial reactivation beneath unfolding buds in branches; 3) inhibition of cambial activity in debudded shoots; and 4) basipetal propagation of cambial reactivation throughout a tree, thereby supporting the classical hypothesis that there is a close connection between cambial reactivation and shoot growth in trees. This hypothesis has generally been accepted; however, some studies have disproved this hypothesis in both conifer and hardwood trees.
For instance, in certain evergreen conifers and deciduous hardwood trees, namely Pinus contorta (Savidge and Wareing, 1981a), Picea sitchensis (Barnett and Miller, 1994), Cryptomeria japonica (Oribe and Kubo, 1997, Begum et al., 2010, Begum et al., 2012), Abies sachalinensis (Oribe et al., 2001), Picea abies (Gričar et al., 2006), A. firma (Begum et al., 2012), Chamaecyparis pisifera (Rahman et al., 2016), Populus sieboldii × P. grandidentata (Begum et al., 2007), and Quercus serrata (Kudo et al., 2014), some experiments have demonstrated that dormant cambium can resume cell division in locally heated stem portions, even during mid-late winter when shoots have not yet started growing. Therefore, sufficient evidence may exist to conclude that a rise in air temperature induces cambial reactivation independently of new shoot growth in trees growing in both the cool-temperate and temperate zones.
However, in our previous study (Oribe and Kubo, 1997), although localized heating of stems over 2 weeks was sufficient to induce cambial reactivation in an evergreen conifer, C. japonica, the same process failed to induce the resumption of cambial cell division in a deciduous conifer, Larix kaempferi. Therefore, there is a need to clarify why cambial reactivation did not occur in stem portions heated for 2 weeks in the deciduous conifer to prove that cambial reactivation can occur independently of shoot growth. In the deciduous hardwood trees of Populus sieboldii × P. grandidentata and Q. serrata, dormant cambium required >4 weeks of localized heating of stems to resume cell division (Begum et al., 2007, Kudo et al., 2014). Deciduous trees might require longer heat treatment as compared with evergreen trees for resumption of cell division in the cambium.
The primary aim of the present study was to demonstrate that cambial reactivation is independent of shoot growth, even in deciduous conifers. Localized heat treatments were applied to stem portions of L. kaempferi at breast height for >2–4 weeks in winter and early spring in a cooler area and warmer area. In the warmer area, stem portions were also locally heated at the crown base. We monitored the extent of cell division in the cambium and differentiation of cambial derivatives in the locally heated stem portions. In the dormant cambium of evergreen conifer trees, its susceptibility to localized heating appeared to depend on climate conditions in the habitats of trees, the date of heating, and its position on the stem (Oribe and Kubo, 1997, Oribe et al., 2001). In addition, to confirm if these findings were applicable to deciduous conifers, we compared responses to the heating of dormant cambium among the treated portions. In our previous studies on locally heated stems of conifers, A. sachalinensis (Oribe et al., 2001, Oribe et al., 2003), C. japonica (Begum et al., 2010), C. pisifera (Rahman et al., 2016), and a hardwood tree, Populus sieboldii × P. grandidentata (Begum et al., 2007), the extent of cambial activity in the locally heated stem portions appeared to depend on sugars supplied from storage starch surrounding the cambium. Therefore, we also observed the localization of storage starch surrounding the cambium during the heating periods to assess growth potential of the dormant cambium under localized heating.
Section snippets
Plant materials and conditions in experimental sites
Larix kaempferi (Lam.) Carrière were used and sourced from the Chiyoda Experimental Station of Forestry and Forest Products Research Institute (36°11′N, 140°13′E) in Ibaraki Prefecture (n = 3) and the Sapporo Experimental Forest of Hokkaido University (43°04′N, 141°20′E) in Hokkaido Prefecture (n = 1) in Japan (Table 1). Larch trees grew sparsely on flat land in both experimental sites. In the Japanese forest soil classification system (Kubo, 1982), soil has been classified as light black soil in
Cambial activity in non-heated samples
In Ibaraki Prefecture, no dividing cambial cells were observed in non-heated samples collected during the period from December 27, 1995 to February 21, 1996 (Fig. 3A–D), indicating that during the first treatment (from December 27, 1995 to January 10, 1996) and the second treatment (from January 24 to February 21, 1996), the cambium was dormant (Table 2). During the third treatment (from February 27 to March 26, 1996), no dividing cambial cells were present in the non-heated samples collected
The requirements for cambial reactivation
As reported by previous studies on evergreen conifers (Savidge and Wareing, 1981a; Barnett and Miller, 1994; Oribe and Kubo, 1997; Oribe et al., 2001; Gričar et al., 2006; Begum et al., 2010; , 2012; Rahman et al., 2016) and deciduous hardwood trees (Begum et al., 2007, Kudo et al., 2014), the dormant cambium of Larix kaempferi is able to resume cell division in locally heated stem portions, even during mid-late winter when shoots had not yet started growing (Table 2). The result suggests that
Acknowledgements
The authors appreciate Dr. T. Kubo, Professor Emeritus, Tokyo University of Agriculture and Technology, making a comment on our study. We are grateful to Dr. Y. Tamai, Faculty of Agriculture in Hokkaido University, and Dr. T. Iki, Tohoku Breeding Office in Forestry and Forest Products Research Institute, for their technical assistance. We would also like to thank Enago (www.enago.jp) for the English language review. This research did not receive any specific grant from funding agencies in the
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