A meta-analysis of cambium phenology and growth: linear and non-linear patterns in conifers of the northern hemisphere

Background and Aims

Ongoing global warming has been implicated in shifting phenological patterns such as the timing and duration of the growing season across a wide variety of ecosystems. Linear models are routinely used to extrapolate these observed shifts in phenology into the future and to estimate changes in associated ecosystem properties such as net primary productivity. Yet, in nature, linear relationships may be special cases. Biological processes frequently follow more complex, non-linear patterns according to limiting factors that generate shifts and discontinuities, or contain thresholds beyond which responses change abruptly. This study investigates to what extent cambium phenology is associated with xylem growth and differentiation across conifer species of the northern hemisphere.

Methods

Xylem cell production is compared with the periods of cambial activity and cell differentiation assessed on a weekly time scale on histological sections of cambium and wood tissue collected from the stems of nine species in Canada and Europe over 1–9 years per site from 1998 to 2011.

Key Results

The dynamics of xylogenesis were surprisingly homogeneous among conifer species, although dispersions from the average were obviously observed. Within the range analysed, the relationships between the phenological timings were linear, with several slopes showing values close to or not statistically different from 1. The relationships between the phenological timings and cell production were distinctly non-linear, and involved an exponential pattern

Conclusions

The trees adjust their phenological timings according to linear patterns. Thus, shifts of one phenological phase are associated with synchronous and comparable shifts of the successive phases. However, small increases in the duration of xylogenesis could correspond to a substantial increase in cell production. The findings suggest that the length of the growing season and the resulting amount of growth could respond differently to changes in environmental conditions.     

Lengthening of the duration of xylogenesis engenders disproportionate increases in xylem production

In cold climates, the expected global warming will lead to earlier cambial resumptions in spring, with a resultant lengthening of the growing season but unknown consequences on forest productivity. The phenological traits of cambium activity and xylem formation were analyzed at a short time scale along a thermal gradient represented by an alti‐latitudinal range from the 48th to 53rd parallels and covering the whole closed black‐spruce [Picea mariana (Mill.) BSP] forest in Quebec, Canada. A hypothesis was tested that warmer temperatures influence cambium phenology, allowing longer duration and higher intensity of growth, and resulting in proportionally increased xylem production. From April to October 2012, cell division in cambium and post‐cambial differentiation of xylem were observed on anatomical sections obtained from microcores collected weekly from the stem of fifty trees. The southern and warmer site was characterized by the highest radial growth, which corresponded to both the highest rates and longest durations of cell production. The differences in terms of xylem phenology and growth were marginal between the other sites. Xylem growth was positively correlated with rate and duration of cell production, with the latter explaining most variability in growth. Within the range analyzed, the relationship between temperature and most phenological phases of xylogenesis was linear. On the contrary, temperature was related with cell production according to an exponential pattern. Periods of xylogenesis of 14 days longer (+13.1%) corresponded to a massive increase in cell production (33 cells, +109%). This disproportionate change occurred at a May–September average temperature of ca. 14 °C and a snow‐free period of 210–235 days. At the lower boundary of the distribution of black spruce, small environmental changes allowing marginal lengthening of the period of cell division could potentially lead to disproportionate increases in xylem cell production, with substantial consequences for the productivity of this boreal species.     

Cambial activity,annual rhythm of xylem production in relation to phenology and climatic factors and lignification pattern during xylogenesis in drum-stick tree (Moringa oleifera)

The interrelationship among seasonality of cambium, wood formation, cell size variation, lignification, tree phenology and climatic factors has been examined in Moringa oleifera, a tropical evergreen tree. The vascular cambium in Moringa is a storied with a distinct seasonal variation in its structure due to dimensional changes in rays. Though cambium remains active throughout the year it is sensitive to water availability. Peak cambial cell division and rate of xylem differentiation are influenced by average rainfall during the monsoon period. Cambial cell division reaches higher up in the tree trunk when it is supporting a high number of branches and leaves. Statistical analysis of cell size variation and climate factors revealed that xylem cell development is greatly influenced by rainfall and rarely by temperature. Lengths of fusiform initials and vessel elements are positively correlated. The pattern of lignification during xylogenesis shows that the vessels are the first element to develop lignified walls and ray cells are the last elements to become lignified. Fiber cell walls show more syringyl lignin, while the cell walls of other xylem elements are characterized by relatively more guaiacyl lignin units.     

Critical temperatures for xylogenesis in conifers of cold climates

Aim To identify temperatures at which cell division and differentiation are active in order to verify the existence of a common critical temperature determining growth in conifers of cold climates. Location Ten European and Canadian sites at different latitudes and altitudes. Methods The periods of cambial activity and cell differentiation were assessed on a weekly time‐scale on histological sections of cambium and wood tissue collected over 2 to 5 years per site from 1998 to 2005 from the stems of seven conifer species. All data were compared with daily air temperatures recorded from weather stations located close to the sites. Logistic regressions were used to calculate the probability of xylogenesis and of cambium being active at a given temperature. Results Xylogenesis lasted from May to October, with a growing period varying from 3 to 5 months depending on location and elevation. Despite the wide geographical range of the monitored sites, temperatures for onset and ending of xylogenesis converged towards narrow ranges with average values around 4–5, 8–9 and 13–14 °C for daily minimum, mean and maximum temperature, respectively. On the contrary, cell division in the cambium stopped in July?August, when temperatures were still high. Main conclusions Wood formation in conifers occurred when specific critical temperatures were reached. Although the timing and duration of xylogenesis varied among species, sites and years, the estimated temperatures were stable for all trees studied. These results provide biologically based evidence that temperature is a critical factor limiting production and differentiation of xylem cells in cold climates. Although daily temperatures below 4?5 °C are still favourable for photosynthesis, thermal conditions below these values could inhibit the allocation of assimilated carbon to structural investment, i.e. xylem growth.     

Hormonal signals involved in the regulation of cambial activity, xylogenesis and vessel patterning in trees

The radial growth of plant stem is based on the development of cribro-vascular cambium tissues. It affects the transport efficiency of water, mineral nutrients and photoassimilates and, ultimately, also plant height. The rate of cambial cell divisions for the assembly of new xylem and phloem tissue primordia and the rate of differentiation of the primordia into mature tissues determine the amount of biomass produced and, in the case of woody species, the wood quality. These complex physiological processes proceed at a rate which depends on several factors, acting at various levels: growth regulators, resource availability and environmental factors. Several hormonal signals and, more recently, further regulatory molecules, have been shown to be involved in the induction and maintenance of cambium and the formation of secondary vascular tissues. The control of xylem cell patterning is of particular interest, because it determines the diameter of xylem vessels, which is central to the efficiency of water and nutrient transport from roots to leaves through the stem and may strongly influence the growth in height of the tree. Increasing scientific evidence have proved the role of other hormones in cambial cell activities and the study of the hormonal signals and their crosstalking in cambial cells may foster our understanding of the dynamics of xylogenesis and of the mechanism of vessel size control along the stem. In this article, the role of the hormonal signals involved in the control of cambium and xylem development in trees and their crosstalking are reviewed.     

Response of xylem formation of Larix sibirica to climate change along the southern Altai Mountains,Central Asia

Under the ongoing warmer and wetter climate in the arid and semi-arid Altai Mountains, the key to understanding and predicting how forest growth responds to the changing climate in this area is to explore the dynamics of xylem formation and its climate drivers. However, such precise and high-time resolution knowledge is currently scarce. Here, we investigated the cambium activity and xylem formation of Siberian larch (Larix sibirica Ledeb.) in four sites along the southern Altai Mountains during the two consecutive growing seasons of 2018 and 2019. We found that the onset of xylem formation along the southern Altai Mountains started from mid-May to early June and ceased from late August to early September. The linear mixed model results showed that the onset of xylogenesis happened earlier when April was warmer and with lower precipitation. The cessation of xylem differentiation was closely related to the total number of xylem cells, regardless of temperature and precipitation. Therefore, a greater number of xylem cells resulted in delayed completion of cell enlargement and wall thickening. In addition, xylem cell production (total number of xylem cells) was negatively affected by May–July temperature and positively affected by May–July total precipitation. Our findings provide key data at the cellular level and high time resolution (weekly) and new insights into how forest ecosystems in the southern Altai Mountains respond to a warmer and wetter climate in the context of global warming.     

Is precipitation a trigger for the onset of xylogenesis in Juniperus przewalskii on the north-eastern Tibetan Plateau?

Background and Aims A series of studies have shown that temperature triggers the onset of xylogenesis of trees after winter dormancy. However, little is known about whether and how moisture availability influences xylogenesis in spring in drought-prone areas.Methods Xylogenesis was monitored in five mature Qilian junipers (Juniperus przewalskii) by microcore sampling from 2009 to 2011 in a semi-arid area of the north-eastern Tibetan Plateau. A simple physical model of xylem cell production was developed and its sensitivity was analysed. The relationship between climate and growth was then evaluated, using weekly wood production data and climatic data from the study site.Key Results Delayed onset of xylogenesis in 2010 corresponded to a negative standardized precipitation evapotranspiration index (SPEI) value and a continuous period without rainfall in early May. The main period of wood formation was in June and July, and drier conditions from May to July led to a smaller number of xylem cells. Dry conditions in July could cause early cessation of xylem differentiation. The final number of xylem cells was mainly determined by the average production rate rather than the duration of new cell production. Xylem growth showed a positive and significant response to precipitation, but not to temperature.Conclusions Precipitation in late spring and summer can play a critical role in the onset of xylogenesis and xylem cell production. The delay in the initiation of xylogenesis under extremely dry conditions seems to be a stress-avoidance strategy against hydraulic failure. These findings could thus demonstrate an evolutionary adaptation of Qilian juniper to the extremely dry conditions of the north-eastern Tibetan Plateau.     

Age-dependent xylogenesis in timberline conifers

Neither anatomical change nor physiological abnormalities have been observed in the cambia of older trees. However, different sensitivity and period of significant responses to climate suggest the existence of some age-related change in the patterns of cambial activity and/or wood cell formation. Here, weekly cambial activity and timing and duration of xylem cell enlargement and wall thickening were compared in adult (50-80 yr) and old (200-350 yr) trees of Larix decidua, Pinus cembra and Picea abies at the Alpine timberline during 2004 and 2005. Timings and durations of xylogenesis differed between adult and old trees, with 2-3 wk shorter cambial activity found in the latter. The delayed onset of cambium division and lower cell production in old trees, with respect to adult trees, led to reductions of 15-20% in the overall duration of xylem differentiation. These results demonstrate that cambial dynamics change during the tree lifespan and that the time window of tree-ring production shortens with age. Variations in the period of xylem growth may be the cause of age-dependent responses to climate. The observed shorter xylogenesis in older plants at the Alpine timberline could be related to a size effect and not just to age per se.     

Cambial activity and intra-annual xylem formation in roots and stems of Abies balsamea and Picea mariana

Background and Aims

Studies on xylogenesis focus essentially on the stem, whereas there is basically no information about the intra-annual growth of other parts of the tree. As roots strongly influence carbon allocation and tree development, knowledge of the dynamics of xylem production and maturation in roots at a short time scale is required for a better understanding of the phenomenon of tree growth. This study compared cambial activity and xylem formation in stem and roots in two conifers of the boreal forest in Canada.

Methods

Wood microcores were collected weekly in stem and roots of ten Abies balsamea and ten Picea mariana during the 2004–2006 growing seasons. Cross-sections were cut using a rotary microtome, stained with cresyl violet acetate and observed under visible and polarized light. The number of cells in the cambial zone and in differentiation, plus the number of mature cells, was counted along the developing xylem.

Key Results

Xylem formation lasted from the end of May to the end of September, with no difference between stem and roots in 2004–2005. On the contrary, in 2006 a 1-week earlier beginning of cell differentiation was observed in the stem, with cell wall thickening and lignification in roots ending up to 22 d later than in the stem. Cell production in the stem was concentrated early in the season, in June, while most cell divisions in roots occurred 1 month later.

Conclusions

The intra-annual dynamics of growth observed in stem and roots could be related to the different amount of cells produced by the cambium and the patterns of air and soil temperature occurring in spring.Key words: Abies balsamea, boreal forest, cambium, cell differentiation, cell wall thickening, lignification, Picea mariana, root, stem, xylem     

Cambial activity and annual rhythm of xylem production of Pinus kesiya Royle ex. Gordon (Pinaceae) in relation to phenology and climatic factors growing in sub-tropical wet forest of North East India

The interrelationship between phenological events, climatic factors, periodicity of cambial activity and seasonal production of xylem was examined in Pinus kesiya Royle ex. Gordon growing in sub-tropical wet forest of Meghalaya state, India. Reactivation of dormant cambium occurs after sprouting of new needles during the middle of February. Since the formation of reproductive cones takes place simultaneously with vegetative bud break and needle formation, cone formation could also lead to the enhancement of cambial activity. The activity of cambium and xylem production decline gradually towards November and cease from end of December to end of January. There was no correlation between needle fall and cambial activity. Due to the production of three flushes of new needles and branches in a year the tree never becomes completely leafless. It was evident from correlation and regression analysis that the annual course of average temperature plays an important role for the reactivation of vascular cambium after dormancy. The differentiation of xylem elements correlated with mean temperature in the first place and secondly with precipitation. Increase in length of fusiform initials and their derivatives could be correlated with relative humidity, precipitation and mean maximum temperature. Dormancy was imposed by low temperature and less precipitation. The data are discussed in the light of cambial activity, xylem production and phenological events.     

Enhancement of secondary xylem cell proliferation by Arabidopsis cyclin D overexpression in tobacco plants

Secondary xylem is composed of daughter cells produced by the vascular cambium in the stem. Cell proliferation of the secondary xylem is the result of long-range cell division in the vascular cambium. Most xylem cells have a thickened secondary cell wall, representing a large amount of biomass storage. Therefore, regulation of cell division in the vascular cambium and differentiation into secondary xylem is important for biomass production. Cell division is regulated by cell cycle regulators. In this study, we confirm that cell cycle regulators influence cell division in the vascular cambium in tobacco. We produced transgenic tobacco that expresses Arabidopsis thaliana cyclin D2;1 (AtcycD2;1) and AtE2Fa-DPa under the control of the CaMV35S promoter. Each gene is a positive regulator of the cell cycle, and is known to influence the transition from G1 phase to S phase. AtcycD2;1-overexpressing tobacco had more secondary xylem cells when compared with control plants. In order to evaluate cell division activity in the vascular cambium, we prepared a Populus trichocarpa cycB1;1 (PtcycB1;1) promoter containing a destruction box motif for ubiquitination and a β-glucuronidase-encoding gene (PtcycB1;1pro:GUS). In transgenic tobacco containing PtcycB1;1pro:GUS, GUS staining was specifically observed in meristem tissues, such as the root apical meristem and vascular cambium. In addition, mitosis-monitoring plants containing AtcycD2;1 had stronger GUS staining in the cambium when compared with control plants. Our results indicated that overexpression of AtcycD enhances cell division in the vascular cambium and increases secondary xylem differentiation in tobacco. Key message We succeeded in inducing cell proliferation of cambium and enlargement of secondary xylem region by AtcycD overexpression. We also evaluated mitotic activity in cambium using cyclin-GUS fusion protein from poplar.     

Influence of exogenous ethylene on cambial activity,xylogenesis and ray initiation in young shoots of Leucaena leucocephala (lam.) de Wit

The effect of exogenous ethephon on cambial activity, xylem production and ray population in young shoots of Leucaena leucocephala was investigated anatomically. The application of ethephon showed a diphasic effect on cambial activity and xylogenesis in a dose dependent manner. Lower concentration of ethephon enhanced cambial activity while high concentrations reduced cambial cell divisions and daughter-cell differentiation. High ethephon concentration also resulted in shorter vessel elements, thick walled fibers and phenolic accumulation in ray cells and vessel elements, whereas low concentration allowed elongation of fibers and vessel elements. The density of rays increased significantly with increase in ethylene concentration. The evaluation of longitudinal sections of cambial zone in ethephon treated plants showed high frequency of transformation of fusiform initials into ray initials through divisions and segmentation, resulting in high ray frequency in both xylem and phloem. The present study demonstrates that ethylene plays an important role in regulating secondary vascular tissue composition by reducing the population of fusiform initials in the cambium.     

Xylem phenology and wood production: resolving the chicken‐or‐egg dilemma

Delays in the start of the growing season reduce the period available for growth and the amount of xylem production. However, a higher number of developing tracheids could prolong cell differentiation and, consequently, lengthen the growing season. The relationship between the amount and duration of cell production in the xylem remains an unresolved issue. The aim of this study was to resolve the chicken‐or‐egg causality dilemma about duration of growth and cell production through simple‐ and double‐cause models. This was achieved by (1) analysing the intra‐annual growth dynamics of the xylem in Picea mariana (Mill.) BSP during 2006–2009 in two contrasting sites of the boreal forest of Quebec, Canada, and (2) extracting the dates of onset and ending of xylem formation and the number of radial cells along the tree ring. A higher number of cells was linked to an earlier onset (r = 0.74) and later ending (r = 0.61) of cell differentiation. The absence of a relationship between the residuals of the onset and ending of xylogenesis (r_p = ?0.06) indicated that cell production influenced the correlation between the two phenophases of the xylem. These results demonstrated that a higher number of cells produced delay the ending of xylem maturation, so extending the duration of wood formation.     

Seasonal development of phloem in Scots pine stems

The formation of phloem was studied for two years in stems of 50 to 60 year old trees of Scots pine (Pinus sylvestris L.) growing in nature. The development of phloem of the current year begins 10 to 20 days before the xylem formation and is completed with the termination of shoot growth in the end of June. Observations over the seasonal activity of cambium producing sieve-like cells of phloem and duration of their differentiation as compared to the xylem derivatives of cambium have shown that the maxima of formation of phloem and xylem cells could coincide or not coincide by season, while the activities of their differentiation were always at antiphase. The sieve-like cells of early phloem were separated from those of late phloem by a layer of tannin-containing cells, which are formed simultaneously with the formation of late xylem cells by the cambium. Seasonal dynamics of accumulation of starch grain in structural elements of the phloem is related to the xylem development. The content of metabolites in differentiating and mature phloem elements, in the cambium zone, and in the xylem cells growing in the radial direction depended on cell specificity, stage of their development, and type of forming wood, early or late, which differ in the cell wall parameters and, hence, requirement of assimilates. Significant differences were described between the content of low molecular weigh carbohydrates, amino acids, organic acids, and phenol compounds using two methods of calculation: per dry weight and per cell.     

水热耦合对沈阳地区油松木质部生长的影响

利用微树芯技术可以从细胞尺度研究树木形成层物候和径向生长的过程,揭示树木生长与气候的关系。油松是我国北方森林的建群树种之一,也是沈阳地区的优势树种。研究2020年整个生长季(4—11月)油松周尺度的形成层及木质部细胞变化,分析油松在沈阳地区的生长规律。结果表明: 油松形成层分裂活动开始于4月初,结束于9月末。木质部从扩大细胞出现(4月中旬)开始生长,到木质化细胞消失(10月下旬)结束,其生长符合“S”型曲线。2020年生长53个/列木质部细胞,最大生长速率(0.55个/列/d)出现在5月末,早晚材细胞于7月末发生转变。在沈阳地区最低温达到0 ℃以上时树木形成层开始活动,影响木质部生长开始和结束的最低临界温度为2～3 ℃。降水在油松整个生长过程中起到促进作用。沈阳地区7月末的高温和水分供给不足是木质部细胞分化形成早晚材的主要因子。     

龙眼剥皮再生的解剖学研究

龙眼(Dimocarpus tongan Lour.)茎干经过大面积环剥,都能再生出新皮。环剥初期,愈伤组织都由近暴露面的射线细胞产生,稍后,其他未成熟木质部细胞也参加愈伤组织的形成,这些愈伤组织一般在靠近表面都可发生木栓形成层,以后迅速形成正常的周皮。在愈伤组织与木质部交界处的未成熟木质部细胞发生维管形成层。新发生的形成层正常地向外分化出次生韧皮部,向内分化出次生木质部。初期有些原来的射线将新形成层带分割成许多小区,二个月后,由于新的形成层不断平周活动,逐渐将形成层连成一圈,以后基本上与正常树皮维管组织的发育一样。     

Seasonal development of phloem in scots pine stems

The formation of phloem was studied for two years in stems of 50 to 60 year old trees of Scots pine (Pinus sylvestris L.) growing in nature. The development of phloem of the current year begins 10 to 20 days before the xylem formation and is completed with the termination of shoot growth in the end of June. Observations over the seasonal activity of cambium producing sieve cells of phloem and duration of their differentiation as compared to the xylem derivatives of cambium have shown that the maxima of formation of phloem and xylem cells could coincide or not coincide by season, while the activities of their differentiation were always in antiphase. The sieve cells of early phloem were separated from those of late phloem by a layer of tannin-containing cells, which are formed simultaneously with the formation of late xylem cells by the cambium. Seasonal dynamics of accumulation of starch grain in structural elements of the phloem is related to the xylem development. The content of metabolites in differentiating and mature phloem elements, in the cambium zone, and in the xylem cells growing in the radial direction depended on cell specificity, stage of their development, and type of forming wood, early or late, which differ in the cell wall parameters and, hence, requirement of assimilates. Significant differences were described between the content of low molecular weigh carbohydrates, amino acids, organic acids, and phenol compounds using two methods of calculation: per dry weight and per cell.     

祁连山中部祁连圆柏年内径向生长对气候因子的响应

通过对祁连山中部葫芦沟流域的祁连圆柏连续采集微树芯,对其形成层活动和径向生长动态进行了连续两年的监测研究。结果表明,2012年细胞壁加厚和细胞成熟阶段开始时间分别发生在6月26日和7月24日,比2013年细胞壁加厚（6月22日）和细胞成熟阶段（6月26日）开始时间分别晚5 d和28 d。2012年细胞扩大、细胞壁加厚和细胞成熟阶段结束时间分别为7月16日、8月9日和9月8日,比2013年各阶段结束时间分别晚7、28 d和24 d。2012年最大细胞分裂速率为0.33细胞/d,共形成20.9个细胞,细胞分裂速率和木质部细胞总数均高于2013年。通过与附近气象站记录的气象数据进行对比,发现祁连圆柏生长开始时间在温暖年份显著早于寒冷年份,说明祁连圆柏的径向生长开始时间与温度有关。但2013年春季和夏初的高温导致区域干旱程度加剧,使祁连圆柏生长结束时间显著早于2012年,并导致2013年的木质部细胞总量和生长速率都小于2012年。研究表明,在寒冷干旱地区,尽管升温会使生长季提前,但升温导致的干旱胁迫可能对树木的生长速率和木质部细胞总量产生重要影响。     

Temperature thresholds for the onset of xylogenesis in alpine shrubs on the Tibetan Plateau

Key message

The threshold minimum air temperature driving xylem growth of alpine  Rhododendron aganniphum is lower than that commonly observed at the treeline of conifers.

Abstract

Understanding how alpine shrubs grow and which environmental factors drive their biomass gain could help to functionally differentiate trees and shrubs. The cambium is the main meristem responsible for wood formation in trees and shrubs. Thus, a better knowledge of cambium growth dynamics in alpine shrubs would allow explaining why shrubs displace trees above the treeline. Here, we aim to investigate the timings and dynamics of xylogenesis and to identify the thermal thresholds controlling the onset of xylem growth of Rhododendron aganniphum, a tall shrub growing above the alpine treeline on the Tibetan Plateau. Timings of xylogenesis and radial growth rates were assessed from anatomical observations of the developing xylem during three growing seasons (2011, 2012, and 2013). The threshold temperature at which xylogenesis had a 0.5 probability of being active was calculated with logistic regressions. The onset of xylogenesis was observed between mid and late June, whereas the end of xylogenesis lasted from mid to late September. Overall, the duration of xylem growth lasted 88–101 days, and 94 % of the ring was formed from June to August. The threshold for the onset of xylem growth was observed at 2.0 ± 0.6 °C for the minimum air temperature, lower than that commonly observed for treeline conifers (ca. 6 °C). This low thermal threshold allows alpine shrubs to have a growing season long enough to complete xylem production and maturation during the warmest summer months. Our results suggest that the time required to complete xylogenesis is critical to understand why shrubs displace trees above the treeline.