High preseason temperature variability drives convergence of xylem phenology in the Northern Hemisphere conifers.

Wood growth is key to understanding the feedback of forest ecosystems to the ongoing climate warming. An increase in spatial synchrony (i.e., coincident changes in distant populations) of spring phenology is one of the most prominent climate responses of forest trees. However, whether temperature variability contributes to an increase in the spatial synchrony of spring phenology and its underlying mechanisms remains largely unknown. Here, we analyzed an extensive dataset of xylem phenology observations of 20 conifer species from 75 sites over the Northern Hemisphere. Along the gradient of increase in temperature variability in the 75 sites, we observed a convergence in the onset of cell enlargement roughly toward the 5th of June, with a convergence in the onset of cell wall thickening toward the summer solstice. The increase in rainfall since the 5th of June is favorable for cell division and expansion, and as the most hours of sunlight are received around the summer solstice, it allows the optimization of carbon assimilation for cell wall thickening. Hence, the convergences can be considered as the result of matching xylem phenological activities to favorable conditions in regions with high temperature variability. Yet, forest trees relying on such consistent seasonal cues for xylem growth could constrain their ability to respond to climate warming, with consequences for the potential growing season length and, ultimately, forest productivity and survival in the future.

PhenoCaB: a new phenological model based on carbon balance in boreal conifers.

Traditional phenological models use chilling and thermal forcing (temperature sum or degree-days) to predict budbreak. Because of the heightening impact of climate and other related biotic or abiotic stressors, a model with greater biological support is needed to better predict budbreak. Here, we present an original mechanistic model based on the physiological processes taking place before and during budbreak of conifers. As a general principle, we assume that phenology is driven by the carbon status of the plant, which is closely related to environmental variables and the annual cycle of dormancy-activity. The carbon balance of a branch was modelled from autumn to winter with cold acclimation and dormancy and from winter to spring when deacclimation and growth resumption occur. After being calibrated in a field experiment, the model was validated across a large area (> 34 000 km2 ), covering multiple conifers stands in Québec (Canada) and across heated plots for the SPRUCE experiment in Minnesota (USA). The model accurately predicted the observed dates of budbreak in both Québec (±3.98 d) and Minnesota (±7.98 d). The site-independent calibration provides interesting insights on the physiological mechanisms underlying the dynamics of dormancy break and the resumption of vegetative growth in spring.

A critical thermal transition driving spring phenology of Northern Hemisphere conifers.

Despite growing interest in predicting plant phenological shifts, advanced spring phenology by global climate change remains debated. Evidence documenting either small or large advancement of spring phenology to rising temperature over the spatio-temporal scales implies a potential existence of a thermal threshold in the responses of forests to global warming. We collected a unique data set of xylem cell-wall-thickening onset dates in 20 coniferous species covering a broad mean annual temperature (MAT) gradient (-3.05 to 22.9°C) across the Northern Hemisphere (latitudes 23°-66° N). Along the MAT gradient, we identified a threshold temperature (using segmented regression) of 4.9 ± 1.1°C, above which the response of xylem phenology to rising temperatures significantly decline. This threshold separates the Northern Hemisphere conifers into cold and warm thermal niches, with MAT and spring forcing being the primary drivers for the onset dates (estimated by linear and Bayesian mixed-effect models), respectively. The identified thermal threshold should be integrated into the Earth-System-Models for a better understanding of spring phenology in response to global warming and an improved prediction of global climate-carbon feedbacks.

The early bud gets the cold: Diverging spring phenology drives exposure to late frost in a Picea mariana [(Mill.) BSP] common garden.

Under climate change, the increasing occurrence of late frost combined with advancing spring phenology can increase the risk of frost damage in trees. In this study, we tested the link between intra-specific variability in bud phenology and frost exposure and damages. We analysed the effects of the 2021 late frost event in a black spruce (Picea mariana (Mill.) BSP) common garden in Québec, Canada. We hypothesised that the timing of budbreak drives the exposure of vulnerable tissues and explains differences in frost damage. Budbreak was monitored from 2015 to 2021 in 371 trees from five provenances originating between 48° and 53° N and planted in a common garden at 48° N. Frost damages were assessed on the same trees through the proportion of damaged buds per tree and related to the phenological phases by ordinal regressions. After an unusually warm spring, minimum temperatures fell to -1.9°C on May 28 and 29, 2021. At this moment, trees from the northern provenances were more advanced in their phenology and showed more frost damage. Provenances with earlier budbreak had a higher probability of damage occurrence according to ordinal regression. Our study highlights the importance of intra-specific variability of phenological traits on the risk of frost exposure. We provide evidence that the timings of bud phenology affect sensitivity to frost, leading to damages at temperatures of -1.9°C. Under the same conditions, the earlier growth reactivation observed in the northern provenances increases the risks of late frost damage on the developing buds.

Environmental and developmental factors driving xylem anatomy and micro-density in black spruce.

Wood density is the product of carbon allocation for structural growth and reflects the trade-off between mechanical support and water conductivity. We tested a conceptual framework based on the assumption that micro-density depends on direct and indirect relationships with endogenous and exogenous factors. The dynamics of wood formation, including timings and rates of cell division, cell enlargement, and secondary wall deposition, were assessed from microcores collected weekly between 2002 and 2016 from five black spruce stands located along a latitudinal gradient in Quebec, Canada. Cell anatomy and micro-density were recorded by anatomical analyses and X-ray measurements. Our structural equation model explained 80% of micro-density variation within the tree-ring with direct effects of wall thickness (σ = 0.61), cell diameter (σ = -0.51), and photoperiod (σ = -0.26). Wood formation dynamics had an indirect effect on micro-density. Micro-density increased under longer periods of cell-wall deposition and shorter durations of enlargement. Our results fill a critical gap in understanding the relationships underlying micro-density variation in conifers. We demonstrated that short-term responses to environmental variations could be overridden by plastic responses that modulate cell differentiation. Our results point to wood formation dynamics as a reliable predictor of carbon allocation in trees.

Comparing the Cell Dynamics of Tree-Ring Formation Observed in Microcores and as Predicted by the Vaganov-Shashkin Model.

New insights into the intra-annual dynamics of tree-ring formation can improve our understanding of tree-growth response to environmental conditions at high-resolution time scales. Obtaining this information requires, however, a weekly monitoring of wood formation, sampling that is extremely time-intensive and scarcely feasible over vast areas. Estimating the timing of cambial and xylem differentiation by modeling thus represents an interesting alternative for obtaining this important information by other means. Temporal dynamics of cambial divisions can be extracted from the daily tree-ring growth rate computed by the Vaganov-Shashkin (VS) simulation model, assuming that cell production is tightly linked to tree-ring growth. Nonetheless, these predictions have yet to be compared with direct observations of wood development, i.e., via microcoring, over a long time span. We tested the performance of the VS model by comparing the observed and predicted timing of wood formation in black spruce [Picea mariana (Mill.)]. We obtained microcores over 15 years at 5 sites along a latitudinal gradient in Quebec (Canada). The measured variables included cell size and the timing of cell production and differentiation. We calibrated the VS model using daily temperature and precipitation recorded by weather stations located on each site. The predicted and observed timing of cambial and enlarging cells were highly correlated (R 2 = 0.8); nonetheless, we detected a systematic overestimation in the predicted timing of cambial cells, with predictions delayed by 1-20 days compared with observations. The growth rate of cell diameter was correlated with the predicted growth rate assigned to each cambial cell, confirming that cell diameter developmental dynamics have the potential to be inferred by the tree-ring growth curve of the VS model. Model performances decrease substantially in estimating the end of wood formation. The systematic errors suggest that the actual relationships implemented in the model are unable to explain the phenological events in autumn. The mismatch between the observed and predicted timing of wood formation in black spruce within our study area can be reduced by better adapting the VS model to wet sites, a context for which this model has been rarely used.

Photoperiod and temperature as dominant environmental drivers triggering secondary growth resumption in Northern Hemisphere conifers.

Wood formation consumes around 15% of the anthropogenic CO2 emissions per year and plays a critical role in long-term sequestration of carbon on Earth. However, the exogenous factors driving wood formation onset and the underlying cellular mechanisms are still poorly understood and quantified, and this hampers an effective assessment of terrestrial forest productivity and carbon budget under global warming. Here, we used an extensive collection of unique datasets of weekly xylem tissue formation (wood formation) from 21 coniferous species across the Northern Hemisphere (latitudes 23 to 67°N) to present a quantitative demonstration that the onset of wood formation in Northern Hemisphere conifers is primarily driven by photoperiod and mean annual temperature (MAT), and only secondarily by spring forcing, winter chilling, and moisture availability. Photoperiod interacts with MAT and plays the dominant role in regulating the onset of secondary meristem growth, contrary to its as-yet-unquantified role in affecting the springtime phenology of primary meristems. The unique relationships between exogenous factors and wood formation could help to predict how forest ecosystems respond and adapt to climate warming and could provide a better understanding of the feedback occurring between vegetation and climate that is mediated by phenology. Our study quantifies the role of major environmental drivers for incorporation into state-of-the-art Earth system models (ESMs), thereby providing an improved assessment of long-term and high-resolution observations of biogeochemical cycles across terrestrial biomes.

How plant allometry influences bud phenology and fruit yield in two Vaccinium species.

BACKGROUND AND AIMS: Understanding how plant allometry, plant architecture and phenology contribute to fruit production can identify those plant traits that maximize fruit yield. In this study, we compared these variables and fruit yield for two shrub species, Vaccinium angustifolium and Vaccinium myrtilloides, to test the hypothesis that phenology is linked to the plants' allometric traits, which are predictors of fruit production. METHODS: We measured leaf and flower phenology and the above-ground biomass of both Vaccinium species in a commercial wild lowbush blueberry field (Quebec, Canada) over a 2-year crop cycle; 1 year of pruning followed by 1 year of harvest. Leaf and flower phenology were measured, and the allometric traits of shoots and buds were monitored over the crop cycle. We hand-collected the fruits of each plant to determine fruit attributes and biomass. KEY RESULTS: During the harvesting year, the leafing and flowering of V. angustifolium occurred earlier than that of V. myrtilloides. This difference was related to the allometric characteristics of the buds due to differences in carbon partitioning by the plants during the pruning year. Through structural equation modelling, we identified that the earlier leafing in V. angustifolium was related to a lower leaf bud number, while earlier flowering was linked to a lower number of flowers per bud. Despite differences in reproductive allometric traits, vegetative biomass still determined reproductive biomass in a log-log scale model. CONCLUSIONS: Growing buds are competing sinks for non-structural carbohydrates. Their differences in both number and characteristics (e.g. number of flowers per bud) influence levels of fruit production and explain some of the phenological differences observed between the two Vaccinium species. For similar above-ground biomass, both Vaccinium species had similar reproductive outputs in terms of fruit biomass, despite differences in reproductive traits such as fruit size and number.

Warming counteracts defoliation-induced mismatch by increasing herbivore-plant phenological synchrony.

Climate change is altering phenology; however, the magnitude of this change varies among taxa. Compared with phenological mismatch between plants and herbivores, synchronization due to climate has been less explored, despite its potential implications for trophic interactions. The earlier budburst induced by defoliation is a phenological strategy for plants against herbivores. Here, we tested whether warming can counteract defoliation-induced mismatch by increasing herbivore-plant phenological synchrony. We compared the larval phenology of spruce budworm and budburst in balsam fir, black spruce, and white spruce saplings subjected to defoliation in a controlled environment at temperatures of 12, 17, and 22°C. Budburst in defoliated saplings occurred 6-24 days earlier than in the controls, thus mismatching needle development from larval feeding. This mismatch decreased to only 3-7 days, however, when temperatures warmed by 5 and 10°C, leading to a resynchronization of the host with spruce budworm larvae. The increasing synchrony under warming counteracts the defoliation-induced mismatch, disrupting trophic interactions and energy flow between forest ecosystem and insect populations. Our results suggest that the predicted warming may improve food quality and provide better growth conditions for larval development, thus promoting longer or more intense insect outbreaks in the future.

The large repertoire of conifer NLR resistance genes includes drought responsive and highly diversified RNLs.

The NLRs or NBS-LRRs (nucleotide-binding, leucine-rich-repeat) form the largest resistance gene family in plants, with lineage-specific contingents of TNL, CNL and RNL subfamilies and a central role in resilience to stress. The origin, evolution and distribution of NLR sequences has been unclear owing in part to the variable size and diversity of the RNL subfamily and a lack of data in Gymnosperms. We developed, searched and annotated transcriptomes assemblies of seven conifers and identified a resource of 3816 expressed NLR sequences. Our analyses encompassed sequences data spanning the major groups of land plants and determinations of NLR transcripts levels in response to drought in white spruce. We showed that conifers have among the most diverse and numerous RNLs in tested land plants. We report an evolutionary swap in the formation of RNLs, which emerged from the fusion of an RPW8 domain to a NB-ARC domain of CNL. We uncovered a quantitative relationship between RNLs and TNLs across all land plants investigated, with an average ratio of 1:10. The conifer RNL repertoire harbours four distinct groups, with two that differ from Angiosperms, one of which contained several upregulated sequences in response to drought while the majority of responsive NLRs are downregulated.

Is size an issue of time? Relationship between the duration of xylem development and cell traits.

BACKGROUND AND AIMS: Secondary growth is a process related to the formation of new cells that increase in size and wall thickness during xylogenesis. Temporal dynamics of wood formation influence cell traits, in turn affecting cell patterns across the tree ring. We verified the hypothesis that cell diameter and cell wall thickness are positively correlated with the duration of their differentiation phases. METHODS: Histological sections were produced by microcores to assess the periods of cell differentiation in black spruce [Picea mariana (Mill.) B.S.P.]. Samples were collected weekly between 2002 and 2016 from a total of 50 trees in five sites along a latitudinal gradient in Quebec (Canada). The intra-annual temporal dynamics of cell differentiation were estimated at a daily scale, and the relationships between cell traits and duration of differentiation were fitted using a modified von Bertalanffy growth equation. KEY RESULTS: At all sites, larger cell diameters and cell wall thicknesses were observed in cells that experienced a longer period of differentiation. The relationship was a non-linear, decreasing trend that occasionally resulted in a clear asymptote. Overall, secondary wall deposition lasted longer than cell enlargement. Earlywood cells underwent an enlargement phase that lasted for 12 d on average, while secondary wall thickness lasted 15 d. Enlargement in latewood cells averaged 7 d and secondary wall deposition occurred over an average of 27 d. CONCLUSIONS: Cell size across the tree ring is closely connected to the temporal dynamics of cell formation. Similar relationships were observed among the five study sites, indicating shared xylem formation dynamics across the entire latitudinal distribution of the species.The duration of cell differentiation is a key factor involved in cell growth and wall thickening of xylem, thereby determining the spatial variation of cell traits across the tree ring.

Contrasting strategies of xylem formation between black spruce and balsam fir in Quebec, Canada.

Present-day global warming is occurring faster at higher elevations. Although there is much information regarding the divergent responses of tree growth to climate change, the altitudinal patterns of species-specific xylogenesis remains poorly understood. We investigated the xylogenesis of balsam fir (Abies balsamea Mill.) and black spruce (Picea mariana Mill. B.S.P.) at two elevations in Quebec (Canada). The number of enlarging and mature cells of the developing tree ring were counted on microcores collected weekly between 2011 and 2014. At the lower site, the growth pattern and duration of xylogenesis were similar between species. No difference in responses to temperature and solar radiation between species was observed. At the higher site, however, cell production was higher and lasted longer in balsam fir than black spruce. Furthermore, the xylem growth of balsam fir had a stronger response to temperature and solar radiation than black spruce. These findings demonstrate the contrasting strategies of wood formation of the two species, with black spruce being more conservative than balsam fir. Our study provides evidence that sympatric species can have species-specific growth dynamics and site-specific responses to the local environment. Predictions of tree growth under a changing environment require the incorporation of species-specific growth strategies.

Phenological shifts in conifer species stressed by spruce budworm defoliation.

Synchrony between host budburst and insect emergence greatly influences the time window for insect development and survival. A few alterations of bud phenology have been reported under defoliation without clear consensus regarding the direction of effects, i.e., advance or delay. Here, we compared budburst phenology between conifers in defoliation and control treatments, and measured carbon allocation as a potential mechanistic explanation of changes in phenology. In a 2-year greenhouse experiment, saplings of balsam fir, black spruce and white spruce of two different provenances (north and south) were subjected to either control (no larvae) or natural defoliation treatment (larvae added) by spruce budworm. Bud and instar phenology, primary and secondary growth, defoliation and non-structural carbohydrates were studied during the growing season. No differences were observed in bud phenology during the first year of defoliation. After 1 year of defoliation, bud phenology advanced by 6-7 days in black spruce and balsam fir and by 3.5 days in white spruce compared with the control. Because of this earlier bud break, apical and shoot growth exceeded 50% of its final length before mature instar defoliation occurred, which decreased the overall level of damage. A sugar-mediated response, via earlier starch breakdown, and higher sugar availability to buds explains the advanced budburst in defoliated saplings. The advanced phenological response to defoliation was consistent across the conifer species and provenances except for one species × provenance combination. Allocation of carbon to buds and shoots growth at the expense of wood growth in the stem and reserve accumulation represents a shift in the physiological resources priorities to ensure tree survival. This advancement in bud phenology could be considered as a physiological response to defoliation based on carbohydrate needs for primary growth, rather than a resistance trait to spruce budworm.

Chilling and forcing temperatures interact to predict the onset of wood formation in Northern Hemisphere conifers.

The phenology of wood formation is a critical process to consider for predicting how trees from the temperate and boreal zones may react to climate change. Compared to leaf phenology, however, the determinism of wood phenology is still poorly known. Here, we compared for the first time three alternative ecophysiological model classes (threshold models, heat-sum models and chilling-influenced heat-sum models) and an empirical model in their ability to predict the starting date of xylem cell enlargement in spring, for four major Northern Hemisphere conifers (Larix decidua, Pinus sylvestris, Picea abies and Picea mariana). We fitted models with Bayesian inference to wood phenological data collected for 220 site-years over Europe and Canada. The chilling-influenced heat-sum model received most support for all the four studied species, predicting validation data with a 7.7-day error, which is within one day of the observed data resolution. We conclude that both chilling and forcing temperatures determine the onset of wood formation in Northern Hemisphere conifers. Importantly, the chilling-influenced heat-sum model showed virtually no spatial bias whichever the species, despite the large environmental gradients considered. This suggests that the spring onset of wood formation is far less affected by local adaptation than by environmentally driven plasticity. In a context of climate change, we therefore expect rising winter-spring temperature to exert ambivalent effects on the spring onset of wood formation, tending to hasten it through the accumulation of forcing temperature, but imposing a higher forcing temperature requirement through the lower accumulation of chilling.

The Physiological Mechanisms Behind the Earlywood-To-Latewood Transition: A Process-Based Modeling Approach.

In extratropical ecosystems, the growth of trees is cyclic, producing tree rings composed of large-lumen and thin-walled cells (earlywood) alternating with narrow-lumen and thick-walled cells (latewood). So far, the physiology behind wood formation processes and the associated kinetics has rarely been considered to explain this pattern. We developed a process-based mechanistic model that simulates the development of conifer tracheids, explicitly considering the processes of cell enlargement and the deposition and lignification of cell walls. The model assumes that (1) wall deposition gradually slows down cell enlargement and (2) the deposition of cellulose and lignin is regulated by the availability of soluble sugars. The model reliably reproduces the anatomical traits and kinetics of the tracheids of four conifer species. At the beginning of the growing season, low sugar availability in the cambium results in slow wall deposition that allows for a longer enlargement time; thus, large cells with thin walls (i.e., earlywood) are produced. In late summer and early autumn, high sugar availability produces narrower cells having thick cell walls (i.e., latewood). This modeling framework provides a mechanistic link between plant ecophysiology and wood phenology and significantly contributes to understanding the role of sugar availability during xylogenesis.

Pattern of xylem phenology in conifers of cold ecosystems at the Northern Hemisphere.

The interaction between xylem phenology and climate assesses forest growth and productivity and carbon storage across biomes under changing environmental conditions. We tested the hypothesis that patterns of wood formation are maintained unaltered despite the temperature changes across cold ecosystems. Wood microcores were collected weekly or biweekly throughout the growing season for periods varying between 1 and 13 years during 1998-2014 and cut in transverse sections for assessing the onset and ending of the phases of xylem differentiation. The data set represented 1321 trees belonging to 10 conifer species from 39 sites in the Northern Hemisphere and covering an interval of mean annual temperature exceeding 14 K. The phenological events and mean annual temperature of the sites were related linearly, with spring and autumnal events being separated by constant intervals across the range of temperature analysed. At increasing temperature, first enlarging, wall-thickening and mature tracheids appeared earlier, and last enlarging and wall-thickening tracheids occurred later. Overall, the period of wood formation lengthened linearly with the mean annual temperature, from 83.7 days at -2 °C to 178.1 days at 12 °C, at a rate of 6.5 days °C-1 . April-May temperatures produced the best models predicting the dates of wood formation. Our findings demonstrated the uniformity of the process of wood formation and the importance of the environmental conditions occurring at the time of growth resumption. Under warming scenarios, the period of wood formation might lengthen synchronously in the cold biomes of the Northern Hemisphere.

Environmental drivers of cambial phenology in Great Basin bristlecone pine.

The timing of wood formation is crucial to determine how environmental factors affect tree growth. The long-lived bristlecone pine (Pinus longaeva D. K. Bailey) is a foundation treeline species in the Great Basin of North America reaching stem ages of about 5000 years. We investigated stem cambial phenology and radial size variability to quantify the relative influence of environmental variables on bristlecone pine growth. Repeated cellular measurements and half-hourly dendrometer records were obtained during 2013 and 2014 for two high-elevation stands included in the Nevada Climate-ecohydrological Assessment Network. Daily time series of stem radial variations showed rehydration and expansion starting in late April-early May, prior to the onset of wood formation at breast height. Formation of new xylem started in June and lasted until mid-September. There were no differences in phenological timing between the two stands, or in the air and soil temperature thresholds for the onset of xylogenesis. A multiple logistic regression model highlighted a separate effect of air and soil temperature on xylogenesis, the relevance of which was modulated by the interaction with vapor pressure and soil water content. While air temperature plays a key role in cambial resumption after winter dormancy, soil thermal conditions coupled with snowpack dynamics also influence the onset of wood formation by regulating plant-soil water exchanges. Our results help build a physiological understanding of climate-growth relationships in P. longaeva, the importance of which for dendroclimatic reconstructions can hardly be overstated. In addition, environmental drivers of xylogenesis at the treeline ecotone, by controlling the growth of dominant species, ultimately determine ecosystem responses to climatic change.

The Contribution of Carbon and Water in Modulating Wood Formation in Black Spruce Saplings.

Nonstructural carbohydrates (NSCs) play a crucial role in xylem formation and represent, with water, the main constraint to plant growth. We assessed the relationships between xylogenesis and NSCs in order to (1) verify the variance explained by NSCs and (2) determine the influence of intrinsic (tissue supplying carbon) and extrinsic (water availability and temperature) factors. During 2 years, wood formation was monitored in saplings of black spruce (Picea mariana) subjected to a dry period of about 1 month in June and exposed to different temperature treatments in a greenhouse. In parallel, NSC concentrations were determined by extracting the sugar compounds from two tissues (cambium and inner xylem), both potentially supplying carbon for wood formation. A mixed-effect model was used to assess and quantify the potential relationships. Total xylem cells, illustrating meristematic activity, were modeled as a function of water, sucrose, and d-pinitol (conditional r(2) of 0.79). Water availability was ranked as the most important factor explaining total xylem cell production, while the contribution of carbon was lower. Cambium stopped dividing under water deficit, probably to limit the number of cells remaining in differentiation without an adequate amount of water. By contrast, carbon factors were ranked as most important in explaining the variation in living cells (conditional r(2) of 0.49), highlighting the functional needs during xylem development, followed by the tissue supplying the NSCs (cambium) and water availability. This study precisely demonstrates the role of carbon and water in structural growth expressed as meristematic activity and tissue formation.