Abstract
Our study investigated the effect of stem temperature increase on xylem formation in Robinia pseudoacacia tree-trunks, caused by direct exposure to solar radiation. It is important to determine factors which may improve the concentricity of deposited wood tissue and intensify xylogenesis because a strong irregularity of wood tissue deposited in the radial direction in mature trees of R. pseudoacacia reduces the commercial value of the wood. Samples of vascular cambium along with adjacent tissues were collected from the southern (illuminated) and northern (shaded) side of tree-trunks growing in the inner and peripheral (thus exposed to direct sunlight) zones of the research plot. Sampling was performed several times during the growing season. The collected material was examined by epifluorescence microscopy and the thickness of deposited tissue comprising cambial xylem derivatives was measured. Deposition of a markedly greater amount of xylem on the southern side of tree-trunks in the peripheral zone of the plot was observed before full leaf development. Instrumental climatic data confirmed that in the early stage of the growing season, temperature on the southern side of the peripheral zone tree-trunk was higher than on the northern side. No clear response in terms of directional deposition of xylem was noticed in the inner zone trees and in peripheral zone trees after full leaf development. This study highlights the importance of temperature increase, caused by solar radiation, for R. pseudoacacia xylogenesis, which may be considered as a factor that affects the course of the radial growth before full leaf development.
Introduction
The vascular cambium produces new layers of secondary xylem and phloem and is composed of two types of initial cells. Axially elongated fusiform initials produce almost all types of xylem and phloem cells, whereas short ray initials produce xylem and phloem ray cells. Cambial activity understood as the occurrence of cell divisions, and thus related to the production of new derivatives, is mostly periodic. There are several factors affecting cambial activity including relative concentration of phytohormones, day length and temperature (Srivastava 1973; Begum et al. 2007; Aloni 2013; Rahman et al. 2018). The key role of temperature in cambial activity was confirmed experimentally. Cambial reactivation and production of new derivatives can be artificially induced by raising the temperature with an externally applied heat source, which was tested in many coniferous trees (Savidge & Wareing 1981; Barnett & Miller 1994; Oribe et al. 2003; Gričar et al. 2006; Begum et al. 2012; Rahman et al. 2016, 2018), the diffuse-porous hardwood hybrid Populus kitakamiensis (P. sieboldii × P. grandidentata) (Begum et al. 2007), and the ring-porous hardwood Quercus serrata (Kudo et al. 2014). Moreover, temperature plays an important role in auxin-mediated growth process — Gray and co-workers (1998) demonstrated that elongation growth of the hypocotyl of Arabidopsis thaliana was significantly greater at 29°C than at 20°C (the study was conducted under constant light conditions — 24 h a day).
As wood is one of the most important raw materials, studying the influence of various factors on cambial reactivation and xylogenesis is essential. The ring-porous hardwood Robinia pseudoacacia is native to North America (Barrett et al. 1990) and grows strongly in Central Europe (Rédei et al. 2002; Wojda et al. 2015). Due to the increasing interest in this species, the study of its radial growth mechanism becomes significant in relation to the production of valuable wood as a raw material (Klisz et al. 2015; Wojda et al. 2015). It can be assumed that when xylogenesis-driving factors exert an influence on the vascular cambium in a uniform manner, meristematic tissue produces a similar amount of secondary xylem along the circumference of a tree-trunk. Theoretically, growth of the cambium is characterized by a circular symmetry (Karczewska et al. 2009). However, if factors affect the cambium unevenly, radial growth may be irregular. It turns out that strong irregularity of deposited tissues in a radial direction may occur in mature trees of R. pseudoacacia, which reduces the commercial value of the wood. From a utilitarian point of view, it seems worth exploring which xylogenesis-driving factors may be controlled in order to improve the concentricity and regularity of deposited wood tissue, as well as to increase the intensity of xylogenesis. To answer the question ‘Which factors affect xylogenesis (the structure and amount of deposited xylem tissue) and to what extent?’ is of key importance in understanding changes occurring in meristematic tissue, and the conditions under which those changes take place. In order to understand the conditions in which cambial derivatives are produced and enlarge, one has to consider a number of factors, including biomechanical and physiological factors.
Taking into account the effect of artificially raised temperature on cambial activity (Savidge & Wareing 1981; Barnett & Miller 1994; Oribe et al. 2003; Gričar et al. 2006; Begum et al. 2007, 2012; Kudo et al. 2014) it was decided to test the influence of temperature increase caused by solar radiation on xylem formation in natural growth conditions. The aim of this study was to investigate to what extent differences in temperature on the southern (illuminated) and northern (shaded) side of deciduous tree-trunks influence the process of xylogenesis, particularly at the beginning of the growing season, before leaf development, in conditions enabling direct exposure of the southern side of a tree-trunk to solar radiation. For this purpose, xylem deposition on different sides of R. pseudoacacia tree-trunks growing in the peripheral and inner zone of the research plot was studied in relation to stem temperature. It was assumed, that the southern side of a tree, which is directly exposed to solar radiation for the longest time during the day, is characterized by a higher temperature, which in turn should result in intensified radial growth at this side of the tree-trunk. Additionally, measurements of the trunk diameter of chosen sample trees were performed with the use of dendrometers, the main phenological events were recorded, and tissues from ca. 3-year-old branches were collected. It is worth noting that if the above-mentioned assumption concerning the influence of tree location within the stand and direct exposure of a given part of a tree-trunk to solar radiation on xylogenesis is true, a sampling method used in studies of cambial derivatives formation should be carefully considered.
Materials and methods
This study was conducted on Robinia pseudoacacia — a deciduous, ring-porous hardwood species. Sample trees (approx. 30-year-old) were selected from a research plot consisting of ca. 150 individual R. pseudoacacia trees (a copse without undergrowth) growing in the Silesian Botanical Garden in the temperate zone of southern Poland (50°10′N, 18°49′E, 331 m above sea level). R. pseudoacacia was selected for the study due to its potential in terms of wood production and because relatively few studies concerning the influence of temperature (raised via artificial heating) on cambial reactivation and xylem deposition have been conducted on broadleaved species, in contrast to conifers.
Collection of plant material
To capture the onset and cessation of xylem formation, the experiment was carried out from 15 Mar. 2015 to 23 Oct. 2015. In order to perform anatomical analysis, three trees located in the inner zone of the plot, namely 20 m from the stand edge (shaded) and three trees located in the southern peripheral part of the plot (exposed to direct sunlight) were selected. Trees from the inner zone were numbered 1, 2 and 3. Trees growing in the outer zone were numbered 4, 5 and 6. These six trees will be termed the main trees (height — approx. 8 m, diameter at breast height — approx. 20 cm). During the growing season, eight samplings of vascular cambium along with adjacent tissues were performed from each of the main trees (Fig. 1). In the case of each sample tree, tissues were collected from the southern, as well as from the northern side of a tree-trunk in a zigzag pattern (0.5–2.0 m above the ground, Fig. 1B). To determine if any disturbances in the process of xylogenesis occurred in the main trees, control samples were also collected from intact trees of the same plot (Fig. 1A). Control samples from intact trees (referred to as control trees) were collected seven times during the growing season, simultaneously with main samplings. Control sampling was not carried out during the first main sampling, as potential disturbances of xylogenesis, induced by multiple sampling, might have occurred only after the first sampling. Additionally, wood samples were collected from eleven reference trees (Fig. 1A). Sampling from reference trees allowed the estimation of the moment of initiation of growth and xylogenesis processes in the main trees, as well as the monitoring of the progression of xylem production in the first part of the growing season. Reference samples were collected before and between the main/control samplings. Reference and control trees had similar diameters to the main trees. Single samples were collected at breast height, from the southern (the most heated) and northern (the least heated) sides of the control and reference tree-trunks.
A: Dates of reference, control and main samplings of Robinia pseudoacacia in 2015. – B: Order of sampling on the southern and northern side of main tree-trunks. – Dates of main and control samplings are emboldened. The main sampling included the collection of tissues from three trees growing in the inner zone and three trees growing in the peripheral zone of the plot. Vascular cambium with adjacent tissues was collected from the southern and northern side of the tree-trunks. Brackets (A) indicate Day of the Year. The black dashed line (B) represents dendrometer measurement.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
Collection of samples containing vascular cambium and adjacent tissues (secondary xylem and phloem) was preceded by removal of periderm with chisel and hammer. Collected tissue fragments (tangential surface — approx. 1.0 × 1.5 cm) were fixed and stored in a glycerol-ethanol mixture (1:1). Samples were cut with a razor blade to the axial dimension of approx. 800 μm resulting in a flattened cuboid shape containing xylem, cambium and phloem cells.
To investigate qualitative differences regarding the deposition of juvenile and mature wood, aside from sampling tree-trunks, fragments of ca. 3-year-old branches were collected. Each of the main samplings included the collection of a single branch from a tree located in the peripheral zone and one from a tree located in the inner zone of the plot. In the case of reference trees, a single branch on each sampling date was collected. All branches were collected from the lower parts of the tree crowns, at a distance of ca. 10 m from the tree-apex.
Measurements of the radial dimension of deposited secondary xylem
Free-hand sections cut with a razor blade were examined by epifluorescence microscopy (Zeiss Lab.A1, FS01 filter, wavelength 365 nm). Observation of unstained material in epifluorescence is possible due to the autofluorescence of lignin, which emits blue light when illuminated with a wavelength of 340–380 nm (Vavrčik et al. 2008). This property is useful in analysing highly lignified xylem tissue. The thickness of deposited tissue comprising cambial xylem derivatives was measured, which was defined as the distance (in a radial direction) between the last growth ring boundary and the initial surface of the vascular cambium. The thickness of deposited xylem tissue was measured in main, control, and reference trees. After cambial reactivation, phloem easily separated from inner tissues (vascular cambium and secondary xylem) and it was difficult to obtain fragments while maintaining full tissue integrity. It was assumed that the line of separation of tissues was in close proximity to the cambial initial surface. This assumption was verified by observation of specimens by phase-contrast microscopy (Olympus BX41). Measurements were performed with OptaView7 software.
Measurements of stem diameter changes
Measurements of the trunk diameter of sample trees (main trees no. 1–3) were performed from 24 Mar. 2015 to 10 Jul. 2015 with the use of manual dendrometers (UMS D1 girth tape). Recordings of the measurements were done at ca. 8 am.
In order to check whether chosen phenological events had an impact on the measured diameters of the tree-trunks, measurement dates have been matched to bud break, full foliage development, flowering, and fructification events. Leaf phenology was monitored from 15 Mar. 2015 to 23 Oct. 2015 in the lower parts of the crowns (at a height of approximately 6 m) at the same time as tissue samples were collected from trees. We adopted (and also modified) phenophases proposed by Sass-Klaassen and co-authors (2011): phenophase 0 — buds in the dormant stage; phenophase 1 — bud brake; phenophase 2 — visible leaves expand; phenophase 3 — leaves fully expanded (Supplementary Data Fig. S1). Flowering and fructification events were monitored in the lower parts of the crown.
Precipitation data acquisition
Daily precipitation was recorded from 5 Mar. 2015 to 23 Oct. 2015 at the Silesian Botanical Garden meteorological station in order to examine if there was a link between precipitation and trunk diameter changes.
Measurements of temperature and relative humidity
In order to verify the assumption that there is a difference in temperature between the illuminated and shaded side of a trunk surface and between trees growing in the peripheral and inner zones of the plot, particularly before full leaf development, stem temperature was measured from 8 May 2015 to 14 Sep. 2015 with HOBO Pro v2 logers (Onset Computer Corporation, Bourne, USA). Temperature and relative humidity were recorded at breast height every hour, on the southern and northern sides of one main tree growing in the peripheral and inner zones of the plot. Temperature/relative humidity sensors in peripheral and inner zone trees were installed slightly below breast height (to enable simultaneous measurements of the trunk diameter changes with the use of a dendrometer in case of the inner zone tree-trunk). Each sensor was carefully placed within the bark groove and stabilised with a screw (see: Supplementary Data Fig. S2) in such a way that it did not cause any damage to the inner bark.
Statistical analysis
To examine deposited xylem thickness (DXT) as a response variable general linear mixed models (GLMM) with a categorical variable GRP (group of trees) at two levels each time, a continuous variable DOY (the day of the year), and a random variable TID (tree ID) were used. Considered GRPs were: the southern side of inner zone trees (123S), the southern side of peripheral zone trees (456S), the northern side of inner zone trees (123N), and the northern side of peripheral zone trees (456N). Models including the DOY variable in linear, square and cubic forms were checked. The model fit was evaluated using the AIC criterion (Akaike 1974). The method of estimating the model parameters (ML, REML, MIVQE0, TYPE3) was fitted to each chosen model separately. Similarly, the structure of the covariance matrix was fitted to each model among matrix structures such as the first-order antedependence, the first-order autoregressive, the heterogeneous first-order autoregressive, the first-order autoregressive moving-average, the compound-symmetry, the heterogeneous compound-symmetry, the Huynh-Feldt covariance, a banded Toeplitz, a heterogeneous banded Toeplitz and an unstructured covariance matrix. The best method of estimation according to the AIC criterion was the restricted maximum likelihood method REML. The significance of the model effects was tested according to the type 3 analysis. For the compared groups of trees, the confidence intervals for the trend of changes in DXT values over time were determined (Patetta 2002). The analyses were done with SAS/STAT 14.3 software, and the MIXED procedure was followed (Littell et al. 2006; SAS Institute 2017).
Results
Temperature and relative humidity on the southern and northern side of tree-trunks
In the initial phase of the growing season (from 8 May 2015 to 22 May 2015; DOY = 128–142) in both outer and inner zones, daily temperatures of trees were higher on the southern side than on the northern side of the tree-trunks (Fig. 2). Daily temperatures measured from 8 May 2015 to 22 May 2015 on the southern side of the trunk surface were higher in the tree growing in the outer zone than in the tree growing in the inner zone of the plot (the difference in maximal day temperature between the southern side of the peripheral zone tree and the southern side of the inner zone tree ranged from 0.7°C to 5.7°C). On the other hand, day temperatures measured on the northern sides of both trunks were similar to each other. From 8 May 2015 to 22 May 2015 temperature differences between the southern and northern sides of a trunk were greater in the tree from the outer zone than in the inner zone.
Differences in temperature and relative humidity between the southern and northern sides of the trunk of a Robinia pseudoacacia tree growing in the peripheral and inner zone of the plot, and also precipitation data obtained from the Silesian Botanical Garden meteorological station from 8 May 2015 to 15 Sep. 2015 (DOY = 128–258). Grey vertical lines indicate the main sampling dates. Temp = temperature. RH = relative humidity. Prec = precipitation. DOY = Day of the Year.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
Later in the growing season (from 23 May 2015 to 14 Sep. 2015; DOY = 143–257) day temperatures in the inner zone tree were similar on both sides of the trunk or were higher on the southern side than on the northern side of the trunk (especially in the second part of July and in August). In the outer zone tree, in June, day temperatures were slightly higher on the southern than on the northern side of the trunk or were similar on both sides of the trunk. From July to mid-August temperatures were higher on the southern or on the northern side or were similar on both sides of the outer zone tree-trunk. From mid-August to mid-September an increase in the temperature difference between the two sides of the trunk of the outer zone tree was noted — day temperatures were higher on the southern side of the trunk.
Temperatures measured on the southern and northern side of the trunks were less diverse during the night than during the day, except for rainy days (Fig. 2). The highest precipitation events reduced the effect of differences in temperature between the southern and northern sides of the tree-trunks.
Peripheral and inner zone trees not only differed in the temperature reached on the southern and northern sides of their trunks but also in relative humidity (Fig. 2). Differences in relative humidity between the two sides of a tree-trunk were predominantly greater in the case of the outer zone tree. The southern side of the peripheral tree-trunk was predominantly characterized by lower values of relative humidity in comparison to the northern side.
Deposited secondary xylem
Before 15 Apr. 2015 no deposition of xylem was observed in both branches and tree-trunks. From 15 Apr. 2015 (fifth reference sampling; DOY = 105) the first lignified vessel elements in branches were observed, which indicated that growth activity had already been taking place (Fig. 3). However, on 15 Apr. 2015 no lignified vessel elements were noticed in the case of a tree-trunk. The first fully lignified vessel elements in a trunk (together with adjacent, lignified cells) were observed on 23 Apr. 2015 (DOY = 113), exclusively in a sample originating from the southern side of the reference tree (Fig. 4). On 30 Apr. 2015 (DOY = 120) the first fully lignified vessel elements along with surrounding lignified cells were also observed on the northern side of a tree-trunk. At the same time, the radial diameter of vessel elements reached 280 μm on the southern side of a tree-trunk, whereas the vessel elements’ radial diameter reached only 160 μm on the northern side. On 7 May 2015 (DOY = 127) the lignification process started in the inter-vessel sections of deposited tissue in a reference tree-trunk/branch, which was considered as a prerequisite for the beginning of the main sampling. Formation of continuous layers of lignified secondary xylem (together with inter-vessel sections) in tree-trunks occurred on 23 May 2015 (DOY = 143). Formation of continuous layers of lignified secondary xylem in branches occurred on 30 May 2015 (DOY = 150). Thus, the formation of lignified vessel elements (together with adjacent cells) precedes lignification of parenchyma cells of the axial and radial system, as well as fibres and tracheids localized between them (Fig. 5).
Transverse sections of secondary xylem and cambial derivatives in samples collected from branches of Robinia pseudoacacia. – A: No newly deposited xylem on 30 Mar. 2015 (DOY = 89). – B: First lignified vessel elements on 15 Apr. 2015 (DOY = 105). – C: Occurrence of continuous layers of lignified secondary xylem on 30 May 2015 (DOY = 150). – Ve = vessel element. Wf = wood fibre. r = ray. Black arrowhead = first lignified vessel element formed in the current growing season. White arrow = unlignified inter-vessel section. White arrowhead = growing vessel element. Black arrow = lignified inter-vessel section. – Scale bars = 100 μm.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
The radial dimension of deposited xylem in main, control and reference trees on the southern and northern sides of the trunks, in the 2015 growing season. Circles = main trees growing in the inner zone of the plot (trees no. 1–3). Squares = main trees growing in the peripheral zone of the plot (trees no. 4–6). Triangles = control trees. Reversed triangles = reference trees. Empty symbols = southern side of a tree-trunk. Filled symbols = northern side of a tree-trunk. DOY = Day of the Year.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
Transverse sections of secondary xylem and cambial derivatives in samples collected on the northern (A, C) and southern (B, D) sides of Robinia pseudoacacia trunks on 23 May 2015 (DOY = 143). – A & B: Micrographs showing tissues collected from tree no. 1, growing in the inner zone of the plot. – C & D: Micrographs showing tissues collected from tree no. 6, growing in the outer zone of the plot. – Ve = vessel element. Wf = wood fibre. r = ray. Black arrowhead = growth ring boundary. Black arrow = lignified inter-vessel section. White arrow = unlignified inter-vessel section. Asterisk = newly formed/forming vessel element. – Scale bars = 200 μm.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
Transverse sections of secondary xylem and cambial derivatives in samples collected on the northern (A, C) and southern (B, D) sides of Robinia pseudoacacia trunks on 23 Jul. 2015 (DOY = 204). – A & B: Micrographs showing tissues collected from tree no. 1, growing in the inner zone of the plot. – C & D: Micrographs showing tissues collected from tree no. 6, growing in the outer zone of the plot. – Ve = vessel element. Wf = wood fibre. r = ray. Black arrowhead = growth ring boundary. White arrowhead = layer of cambial initials. – Scale bars = 500 μm.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
In 88 percent of samplings of outer zone trees (eight main samplings, three trees each) there was a predominance of radial growth on the southern side of the tree-trunk (Supplementary Data Table S1). In the case of the first four samplings, more xylem was deposited on the southern side of peripheral zone tree-trunks (Fig. 4; Fig. 5C, D). Differences in the amount of deposited xylem between the southern and northern sides were especially pronounced from 8 May 2015 to 23 May 2015 (DOY = 128–143; evident in all three trees of the outer zone). In the case of two peripheral trees (nos. 5 and 6) the difference between xylem deposition on the southern and northern side of a trunk was highly reduced on 23 Jun. 2015 (DOY = 174; Fig. 6C, D). Only one tree from the peripheral zone (no. 4) showed a uniform trend of deposition of greater amounts of secondary xylem on the southern side throughout the whole growing season. In the case of trees no. 5 and 6, more deposited xylem was observed on the southern or northern side of their trunks after 23 Jun. 2015 (DOY = 174; Fig. 4). The last sampling (23 Oct. 2015; DOY = 296) revealed much more deposited secondary xylem on the southern than on the northern side of tree no. 4 (a difference of 1287 μm), tree no. 5 had more deposited xylem on the southern side of the trunk (a difference of 404 μm), while tree no. 6 had slightly more deposited xylem on the northern side of the trunk (a difference of 87 μm). Interestingly, despite the fact that after the first four samplings peripheral tree-trunks did not show a common tendency for deposition of a greater amount of xylem on one side, as at the beginning of the growing season, all three trees reacted similarly in terms of deposition of a greater amount of xylem on the southern side of their trunks on 23 Aug. 2015 (DOY = 235).
The distance between the initial layer and the growth ring boundary was larger on the southern side of all reference trees (Fig. 4; Supplementary Data Table S1) — differences in the thickness of deposited xylem between the southern and northern side of individual tree-trunks ranged from 21 μm to 589 μm. In the case of control trees, larger amounts of deposited xylem were noted on the southern or on the northern side of a tree-trunk (Fig. 4; Supplementary Data Table S1).
There was no prolonged predominance of deposited xylem tissue on the northern or southern side of R. pseudoacacia trees growing in the inner zone of the plot (Fig. 5A, B; Fig. 6A, B). In 50 percent of samplings from trees growing in the inner zone (eight main samplings, three trees each) a greater radial growth (understood as cambial derivatives deposited on the xylem side) was noted on the southern side of a tree-trunk (Supplementary Data Table S1). All trees of the inner zone of the plot finished their growth with a larger xylem increment on the northern side (Fig. 4).
Models (with 95 % confidence intervals) of thickness changes of deposited xylem over time for compared groups of trees (A−F). – A: Southern sides of inner zone trees and northern sides of peripheral zone trees. – B: Northern sides of inner zone trees and southern sides of peripheral zone trees. – C: Southern sides of inner zone trees and southern sides of peripheral zone trees. – D: Northern sides of inner zone trees and northern sides of peripheral zone trees. – E: Northern and southern sides of peripheral zone trees. – F: Northern and southern sides of inner zone trees. – 123N = northern sides of inner zone trees. 123S = southern sides of inner zone trees. 456N = northern sides of peripheral zone trees. 456S = southern sides of peripheral zone trees. DXT = deposited xylem thickness. DOY = Day of the Year.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
Results of the linear mixed models to test for differences in the thickness of deposited xylem in time due to comparisons of groups of trees, chosen forms of the model and the covariance matrix structure and P-value for comparisons of groups of trees.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
A comparison of groups of main trees (Fig. 7 and Table 1), based on chosen models, showed that until the 220th day of the year, differences between the thickness of deposited xylem on the southern sides of peripheral and the inner zone tree-trunks were significant — later in the growing season confidence intervals overlap. Significant differences in the amount of deposited xylem were also found between the northern side of inner zone tree-trunks and the southern side of peripheral zone tree-trunks until the 180th day of the year — later in the growing season confidence intervals overlap. All other comparisons of the groups of trees examined showed no significant differences.
The anatomical analysis showed no substantial difference in juvenile wood deposition between branches originating from reference trees, as well as from inner and peripheral zone main trees. Lignification of vessel elements in branches occurred earlier than in tree-trunks.
A, B & C: Dendrometers recordings showing Robinia pseudoacacia trunk diameter changes from 24 Mar. 2015 to 10 Jul. 2015 (DOY = 83–191). – D: Precipitation data obtained from the Silesian Botanical Garden meteorological station from 24 Mar. 2015 to 12 Jul. 2015 (DOY = 83–193). – A = tree no. 1. B = tree no. 2. C = tree no. 3. Prec = precipitation. DOY = Day of the Year.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
Reference, control and main samplings, and phenological/anatomical events considered during the study. The study covers the time-span from March 2015 to October 2015. Days of the year of main and control samplings are emboldened. VE = lignified vessel elements in a tree-trunk. ve = lignified vessel elements in a branch. BB = bud break. EL = expanding leaves. L = leaves fully developed. f = flowering. F = fructification.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
Tree-trunk diameter changes
There were three periods when a pronounced decrease of trunk diameter was noticed in all three examined trees (Fig. 8). The first one occurred in the first half of April (DOY = 93–104 for trees no. 1 and 2; DOY = 93–103 for tree no. 3), the second at the end of May and at the beginning of June (DOY = 148–153 for trees no. 1 and 2; DOY = 149–153 for tree no. 3), and the third at the end of June and at the beginning of July (DOY = 181–187 for trees no. 1 and 2; DOY = 184–188 for tree no. 3). The first reduction of measured diameters of tree-trunks preceded the formation of the first lignified vessel elements in branches, which was observed in a reference tree on 15 Apr. 2015 (DOY = 105; Fig. 9). The second reduction coincided with full leaf development and flowering (Fig. 9), both of which were observed in a reference tree on 30 May 2015 (DOY = 150). The third reduction of diameters coincided with a short-term lack of precipitation. The period of precipitation deficiency lasted from 30 Jun. 2015 to 7 Jul. 2015 (DOY = 181–188; Fig. 8). All of the three dendrometers recorded several periods of a pronounced increase in tree-trunk diameter, which coincided with the occurrence of precipitation (Fig. 8).
Discussion
An effect of temperature on xylogenesis in tree-trunks in natural conditions
It is well known that temperature affects cambial activity including occurrence of cell divisions and formation of derivatives (Savidge & Wareing 1981; Barnett & Miller 1994; Oribe et al. 2003; Gričar et al. 2006; Begum et al. 2007, 2012; Kudo et al. 2014; Rahman et al. 2016, 2018). In the present study it was assumed that temperature increase, caused by solar radiation, may affect xylogenesis in natural growth conditions — a side of a tree which is directly exposed to solar radiation for a longer period of time during the day would have a higher temperature, which in turn should result in intensified radial growth. Thus, the xylogenesis process would be promoted on this side of the tree-trunk. In accordance with the above-mentioned assumption it was revealed that, before the full development of leaves of the peripheral zone tree, the southern side of its trunk had a higher temperature than the northern side. At the same time (8 May 2015 to 22 May 2015; DOY = 128–142), day temperatures on the southern side of a trunk were higher in the tree from the peripheral zone than in the tree from the inner zone of the plot. R. pseudoacacia trees have relatively thick bark, which may be considered as an insulation layer for inner living tissues against external (biotic/abiotic) factors. However, bark in this species varies strongly in terms of radial thickness. In some locations around a trunk circumference, it may be as thick as 15 mm, while in other locations it may be very thin — ca. 1 mm in grooves (in trees used in this study). As was indicated in the materials and methods, HOBO sensors were placed within the grooves. One may suspect that solar radiation will influence phloem and vascular cambium predominantly through these grooves. The previously mentioned stronger heating of the southern side of the peripheral zone tree resulted in a decrease in relative humidity on that side (Fig. 2). In this period of the vegetative season, trees from the outer zone showed larger growth on the southern (illuminated) side of their trunks. In all three examined trees, in the case of the first three samplings, a clear predominance of the amount of deposited xylem tissue was observed on the southern side of the trunks. At this point, it should be explained how temperature differences between the southern and northern sides of a trunk in the first part of the growing season, before full development of foliage, could affect conditions occurring in specific parts of a tree-trunk. Firstly, one should consider the influence of temperature on auxin level — temperature-induced increase in the level of auxin was observed for Arabidopsis thaliana (Gray et al. 1998; Franklin et al. 2011; Sun et al. 2012). Auxin is a strong stimulator of both cambial activity and xylem differentiation (Zakrzewski 1983; Wodzicki 1993; Uggla et al. 1998) and is involved in cell growth, as is explained, for example, by the acid growth hypothesis (Hager et al. 1971; Rayle & Cleland 1992). Kudo and co-authors (2014) showed that reactivation of vascular cambium, as well as differentiation of first vessel elements in the ring-porous species Quercus serrata does not depend upon auxin supply from the buds — both processes occurred in disbudded, heat-treated seedlings. The level of endogenous auxin in quiescent cambium might be sufficient for both cambial reactivation and differentiation of the first cambial derivatives (Kudo et al. 2014). Examination of a ring-porous species Ulmus glabra revealed the presence of auxin precursors in a tree-trunk prior to bud opening (Digby & Wareing 1966). It is worth noting that a field experiment conducted on Populus tremula showed that expression of genes encoding auxin transporters increases when temperatures stay above 0°C for several days (Schrader et al. 2003). Secondly, the influence of temperature can be considered in relation to changes related to thermal expansion of materials, changes in osmotic potential of cells, changes in enzymatic activity, or influence on various physiological reactions. It is known that changes in temperature and osmolarity of the cell environment cause fluctuations of cell membrane fluidity (Los & Murata 2004). It may be presumed that such fluctuations obviously influence the strain of the cell membrane. Mechanical stress in the cell wall and cellular signalling are in turn influenced by osmotic phenomena and associated adaptive reactions termed osmoregulation (Alexandre & Lassalles 1991; Felix et al. 2000; Zhang et al. 2007; Hamann et al. 2009; Kurusu et al. 2012a, b; Nakayama et al. 2012; Veley et al. 2012; Wormit et al. 2012; Monshausen & Haswell 2013). It can be speculated that thermal energy, permeating osmotically active tissues/cells which are capable of osmotic adaptation, contributes to generation of mechanical stress through an increase in the osmotic potential of cells (for instance as a consequence of hydrolysis of starch and increase in concentration of osmotically active substances), thus enabling water influx into osmotically active (living) cells. The disappearance of starch in artificially heated stems was observed in Chamaecyparis pisifera (Rahman et al. 2016) and hybrid Populus sieboldii × Populus grandidentata (Begum et al. 2007). How is generated mechanical stress linked to the growth of cambial derivatives? To answer this question, one should take into account the relation between mechanical stress and auxin. It has been found that mechanical stress affects polar transport of auxin by changing the location of its polar transport carriers — PIN proteins (Paciorek et al. 2005; Dhonukshe et al. 2007; Heisler et al. 2010; Nakayama et al. 2012). Moreover, an increase in mechanical strain leads to an overall increase in the number of PIN1 transporters in cells, inside cells and in cell membranes (Nakayama et al. 2012). Finally, the hydrolysis of starch may not only change osmotic potential of cells and thus their hydration, which affects mechanical stress, but also it may influence auxin biosynthesis — it was observed that a higher concentration of dissolved sugars promotes auxin biosynthesis in cells (Lilley et al. 2012; Sairanen et al. 2012).
According to the reasoning presented so far, it can be presumed that before the full development of leaves, the temperature would influence the level of auxin (Gray et al. 1998) and would indirectly contribute to generation of mechanical stress. Mechanical stress may, in turn, affect hormonal regulation (Nakayama et al. 2012), thereby also inducing/intensifying the xylogenesis process. It might explain deposition of greater amounts of xylem on the southern side of tree-trunks of peripheral zone trees during the early growing season. However, despite the fact that before full development of leaves, the tree of the inner zone also showed higher temperatures on the southern side of its trunk (Fig. 2), there was no prolonged prevalence of xylem tissue deposition at any side of a trunk in case of trees located in the inner part of the plot. It can be assumed that due to the location (partial obscuration by other trees) the temperature reached on the southern sides of trunks of inner zone trees was not sufficient to cause prolonged and pronounced intensification of xylogenesis. A presumption about the stimulating role of temperature increase (caused by solar radiation) on xylogenesis intensification is consistent with the statistical significance of differences between thickness of deposited xylem on the southern sides of inner and peripheral zone trees, and also between the northern sides of inner zone trees and the southern sides of peripheral zone trees in the first part of the growing season, before the 220th and 180th day of the year respectively.
In the later part of the growing season, after the leaves were fully developed, there was no clear eccentric growth, in comparison to the beginning of the growing season, in peripheral zone trees. Only tree no. 4 showed a clear predominance of xylem tissue deposition on the southern side of the trunk throughout the whole growing season. Interestingly, all outer zone trees deposited more xylem tissue on the southern sides of their trunks on 23 Aug. 2015 (DOY = 235), during the period of an increase in temperature difference between the two sides of the trunk of the outer zone tree (from mid-August to mid-September). However, on 23 Sep. 2015 (after the termination of a period of increased heating of the southern side of a trunk; DOY = 266) in tree no. 6 the predominance of deposited xylem occurred on the northern side. Also, in case of trees growing in the inner zone of the plot no clear, prolonged predominance of deposition of xylem tissue on the southern or northern side of a tree-trunk was observed after the full development of leaves. It may be speculated that after full development of leaves, the influence of temperature on xylogenesis is not as significant as in the leafless state due to transpiration-driven diurnal deformations (Kojs & Rusin 2011). Diurnal cycles of shrinkage and swelling of plant organs are well documented (Kozlowski & Winget 1964; Klepper et al. 1971; Simonneau et al. 1993; Ueda & Shibata 2001; Yoshida et al. 2003). Their nature is much more circularly symmetric than the influence of solar radiation, which may be regarded as close to unidirectional (particularly in the early part of the growing season). It is thought that shrinkage of tissues is related to transpiration, which causes a decrease in water potential in conductive elements and results in a decrease in cell hydration (Kojs & Rusin 2011). Detailed studies showed that the shrinkage almost exclusively concerns elastic tissues (mainly phloem, cambium, parenchyma) and that the radial dimension of tissue depends upon water content (Zweifel et al. 2000). Nonetheless, an impact of xylem on trunk mechanics should not be ignored (Alméras et al. 2006), because, as has been shown, the uptake of water occurs also from xylem, which has low elasticity (Zweifel et al. 2000). Another explanation of the phenomena observed may be the simultaneous influence of various factors on xylogenesis. For example, influence of trunk inclination may be considered (Hellgren et al. 2004; Groover 2016; Aiso et al. 2017). It is worth noting that the peripheral zone trees were characterized by a slightly greater deviation from a vertical position in comparison to inner zone trees. All three trees from the outer zone of the plot were inclined toward an S–SE direction. In such a situation, radial growth at the stretched sides of tree-trunks (N–NW) should be promoted (Groover 2016; Aiso et al. 2017). Interestingly, tree no. 4, which showed a consistent tendency for markedly greater xylem deposition on the southern side of its trunk, was the one with the smallest inclination (among peripheral zone trees). It might be assumed that due to the smallest deviation from a vertical position (among peripheral zone trees) influence of temperature on xylogenesis should be the most pronounced in tree no. 4. The already mentioned deposition of greater amount of xylem on the southern sides of all peripheral tree-trunks (23 Aug. 2015; DOY = 235) in the period of stronger heating of the southern side of the outer zone trunk (Fig. 2) may be explained by a temperature increase countering the influence of mechanical forces resulting from trunk inclination. It is also possible that both explanations are correct: effect of temperature increase, caused by solar radiation, on the deposition of xylem is not as strong as in the leafless state, due to transpiration-driven diurnal deformations (Kojs & Rusin 2011) and by the simultaneous influence of other factors such as inclination of a tree-trunk (Hellgren et al. 2004; Groover 2016; Aiso et al. 2017). It is worth noting that no significant differences between southern sides of peripheral and inner zone trees occurred after the 220th day of the year and between the southern sides of peripheral zone trees and the northern sides of inner zone trees after the 180th day of the year. It can be assumed that lack of statistically significant differences in the later part of the growing season may be related to the reduction of temperature influence on xylogenesis on the southern sides of peripheral zone tree-trunks because of the above-mentioned reasons. In order to elucidate an effect of temperature increase, caused by solar radiation, on xylogenesis after full leaf development further studies are necessary.
In the light of this study, it can be stated that solar radiation received and the resulting increase in temperature is important for initiation/intensification of the xylogenesis process in R. pseudoacacia in the early part of the growing season — before the full development of foliage.
The onset of xylogenesis in branches and trunks
It was noted that lignification of vessel elements in R. pseudoacacia occurred earlier in branches than in tree-trunks, which confirmed the results reported in other studies performed on ring-porous species (Takahashi et al. 2013; Kudo et al. 2015; Kitin & Funada 2016). Perhaps earlier formation of vessel elements in branches (Fig. 3) is related to the greater responsiveness of vascular cambium to solar radiation, due to a relatively thin periderm in branches. If true, earlier initiation of cell differentiation in branches would be related to the proposed temperature-driven response, which includes an influence on the level of auxin (Gray et al. 1998) and auxin transport regulation through mechanical stress (Nakayama et al. 2012).
Practical remarks based on examination of xylogenesis in R. pseudoacacia tree-trunks
Some practical tips concerning the improvement of tree-trunk concentricity and selection of the most suitable sampling method in studies of cambial activity and/or formation of cambial derivatives in trees may be given on the basis of the conducted study. As uneven deposition of xylem occurred at the beginning of the growing season in peripheral zone tree-trunks (due to uneven heating of the stem), improvement of the concentricity of tree-trunks by planting R. pseudoacacia trees in mixed stands with evergreen tree species such as Picea, is worth considering. Individuals of the selected evergreen species should be adequately younger and/or lower than planted R. pseudoacacia trees in order to create an under-canopy layer and to shade R. pseudoacacia tree-trunks, but not their crowns. Another suggestion may be planting R. pseudoacacia trees with adequately younger deciduous tree species characterized by earlier leaf development and withstanding partial shade. As Panchen and co-authors (2014) indicated, on average, diffuse- and semi-ring-porous species leaf out earlier than ring-porous ones. Similar observations concerning the timing of bud break in ring- and diffuse-porous species may be found in many articles (Aloni & Peterson 1997; Frankenstein et al. 2005). Thus, it seems that R. pseudoacacia, being one of the latest leaf flushing trees in Central Europe, may be planted not only with eligible evergreen species, but also some deciduous trees, especially diffuse-porous ones.
Studies on cambial reactivation and commencement of production of cambial derivatives in ring- and diffuse-porous trees have recently gained popularity (Frankenstein et al. 2005; Takahashi et al. 2013; Kudo et al. 2015; Puchałka et al. 2017). Our results indicate the need for paying special attention to the sampling method used in studies concerning cambial activity and cambial derivatives formation, especially at the beginning of the growing season. In view of differences in the amount of deposited xylem tissue between the southern and northern sides of peripheral zone tree-trunks (clearly noticeable before full leaf development), location of trees within the stand, as well as orientation of a given part of a tree-trunk relative to the cardinal directions should be considered when sampling cambium and adjacent xylem of ring-porous trees.
Heterogeneity in the thickness of deposited xylem
It is known that wounding of a trunk results in structural changes in the vicinity of the wound (Frankenstein & Schmitt 2006). Therefore, one should consider whether multiple sampling may have led to the disruption of polar, basipetal auxin transport (Aloni 2013) and thus to disturbances of xylogenesis in areas located below locations of previous sampling. To avoid disturbances in the process of xylogenesis, samples were collected in a zigzag pattern, 0.5–2.0 m above the ground. Additionally, each time, a distance of several centimetres between successive sampling areas was maintained. Nonetheless, a smaller amount of deposited xylem tissue in relation to the previous sampling was observed in several cases, especially in the later part of the growing season. Some of these cases might have been caused by disturbances of xylogenesis as a result of multiple sampling whereas other cases, considering sampling order and location of tissue collection areas, do not appear to be caused by disruption of xylogenesis. Instead, it appears that in different parts of a tree-trunk various amounts of xylem may be deposited. Therefore, it seems that further studies on the mechanism of radial growth in deciduous trees may explain local differences in the formation of secondary tissues. A comparison of control trees to main trees leads to the conclusion that the main trees did not show substantial differences when it comes to the dynamics of deposited xylem tissue. Even if some disturbances occurred as a result of multiple sampling from the same tree, a clear difference in growth reactions between trees of the peripheral and inner zones is noticeable at the beginning of the growing season before full development of leaves.
Stem diameter changes
During the 2015 growing season, three outstanding periods of diameter reduction were observed in trunks of all the examined R. pseudoacacia trees. The first reduction preceded xylogenesis initiation in branches. This event might have been associated with changes in water relations within and between the tissues (Zweifel et al. 2000). The second reduction was associated with the full development of leaves and flowering. It should be considered that the full development of leaves is associated with an intensification of the transpiration process, which would contribute to the periodic reduction of tissue hydration and cause reversible shrinkage of the stem (Simonneau et al. 1993). A reduction of tissue hydration and consequently a change of tissue osmotic potential as well as mechanical conditions within a tree-trunk could entail a decrease in radial growth intensity. While considering effects caused by leaf development on radial growth phenomena, it is worth to note that some researchers observed a decrease in cambial activity and wood deposition rate, which they proposed to be a result of carbohydrate depletion that has been used for the earlywood formation, as well as leaf development (Michelot et al. 2012; Puchałka et al. 2017). Michelot et al. (2012) noticed a large decrease in starch from April to June, as well as a relatively small deposition of wood in May (representing 13 percent of the ring width), following greater deposition of wood in April in Quercus petraea (budburst occurred around mid-April). Puchałka and co-authors (2017) observed a decrease in the number of cell layers in the vascular cambium of Quercus robur in May. Leaves were nearly fully developed at the end of April and at the beginning of May. The third reduction could be related to temporary lack of precipitation and reduction of water availability (Fig. 8). Reduced water availability and ongoing transpiration result in a decrease in tissue hydration, which is responsible for the observed shrinkage of a tree-trunk (Simonneau et al. 1993; Kojs & Rusin 2011). During the conducted study several periods of increase in tree-trunk diameters were observed. Considerable increase of tree-trunk diameters occurred in the periods of abundant precipitation. It can be assumed that increased water availability, through an increase in tissue hydration, is responsible for generating strong mechanical stress, which could entail radial growth intensification. Therefore, growth may be considered as plastic deformation of tissues, as opposed to elastic deformation, which is reversible (Alméras et al. 2006; Cosgrove 2018). Both deformations are related to the swelling of tissues in a tree-trunk.
Conclusions
In this study deposition of a markedly greater amount of xylem tissue was observed on the southern sides of tree-trunks growing in the peripheral zone of the plot early in the growing season (before the full development of leaves). Our experiment confirmed that the temperature on the southern side of the outer zone tree, which was directly exposed to solar radiation, was higher in comparison to the northern side at the early stage of the growing season. It can be speculated that before leaves fully develop, temperature may influence, for example, the level of auxin and/or generated mechanical stress which affects hormonal regulation, thereby inducing/intensifying the process of xylogenesis. In the case of trees growing in the inner zone of the plot, no prolonged predominance of deposition of xylem tissue on the southern or northern sides of a tree-trunk was observed. Our studies confirmed the hypothesis that, due to partial obscuration by other trees, temperature values reached on the southern sides of the inner zone tree-trunks were not sufficiently high for an intensification of the xylogenesis process, in contrast to the tree-trunks located in the peripheral zone. After the full development of leaves in both inner and outer zone trees, no prolonged predominance of deposition of xylem tissue was noticed (with the exception of one peripheral tree). It can be postulated that after the full development of leaves the influence of temperature on mechanical conditions inside a tree-trunk is not as strong as in the leafless state, due to the occurrence of transpiration-driven diurnal deformations and/or the influence of other factors such as tree-trunk inclination. Thus, it seems that received solar radiation is a factor influencing the course of xylogenesis (amount of deposited xylem tissue) at the first stage of the growing season, before the full development of leaves. Finally, improvement of concentricity of tree-trunks by planting R. pseudoacacia trees in mixed stands with evergreen tree species, such as Picea sp., is worth taking into consideration. Individuals of the selected species should be adequately younger than planted R. pseudoacacia trees in order to shade R. pseudoacacia tree-trunks, but not their crowns.
Corresponding author; email: a.miodek@obpan.pl
Acknowledgements
This work was supported by the General Directorate of State Forests in Poland [grant number BLP 386] and linked to activities conducted within the COST FP1403 ‘NNEXT’ network. We thank David Oldroyd for linguistic corrections of the text.
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Footnotes
Associate Editor: Lloyd Donaldson
Appendix Supplementary data
Leaf phenophases of Robinia pseudoacacia. – A: Buds in dormant stage on 23 Apr. 2015 (DOY = 82; phenophase 0). – B: Beginning of bud break on 23 Apr. 2015 (DOY = 113; phenophase 1). – C: Visible leaves expand on 30 Apr. 2015 (DOY = 120; phenophase 2). – D: Leaves are fully expanded on 30 May 2015 (DOY = 150; phenophase 3). – The phenophases described are adopted (and also modified, i.e. phase of bud swelling is omitted) from Sass-Klaassen et al. (2011). – Scale bars = 2 cm.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
Measurements of temperature and relative humidity on the southern side of the peripheral zone tree-trunk. Second temperature/relative humidity sensor was placed on the other side of the tree-trunk.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
Radial dimension of deposited xylem derivatives in main (T1–T6), control (CT) and reference (RT) trees on the southern (S) and northern (N) sides of a trunk in the 2015 growing season.
Citation: IAWA Journal 41, 1 (2020) ; 10.1163/22941932-00002106
