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Despite considerable experimental effort, the physiological mechanisms governing temperate tree species' water and carbon dynamics before the onset of the growing period remain poorly understood. We applied 2 H-enriched water during winter dormancy to the soil of four potted European tree species. After 8 weeks of chilling, hydrogen isotopes in stem, twig and bud water were measured six times during 2 consecutive weeks of forcing conditions (Experiment 1). Additionally, we pulse-labelled above-ground plant tissues using 2 H-enriched water vapour and 13 C-enriched CO 2 7 days after exposure to forcing conditions to trace atmospheric water and carbon uptake (Experiment 2). Experiment 1 revealed soil water incorporation into the above-ground organs of all species during the chilling phase and significant species-specific differences in water allocation during the forcing conditions, which we attributed to differences in structural traits. Experiment 2 illustrated water vapour incorporation into all above-ground tissue of all species. However, the incorporation of carbon was found for evergreen saplings only. Our results suggest that temperate trees take up and reallocate soil water and absorb atmospheric water to maintain sufficient above-ground tissue hydration during winter. Therefore, our findings provide new insights into the water allocation dynamics of temperate trees during early spring., (© 2024 The Author(s). Plant, Cell & Environment published by John Wiley & Sons Ltd.)

Earlier spring growth onset in temperate forests is a visible effect of global warming that alters global water and carbon cycling. Consequently, it becomes crucial to accurately predict the future spring phenological shifts in vegetation under different climate warming scenarios. However, current phenological models suffer from a lack of physiological insights of tree dormancy and are rarely experimentally validated. Here, we sampled twig cuttings of five deciduous tree species at two climatically different locations (270 and 750 m a.s.l., ~ 2.3 °C difference) throughout the winter of 2019-20. Twig budburst success, thermal time to budburst, bud water content and short-term 2H-labelled water uptake into buds were quantified to link bud dormancy status with vascular water transport efficacy, with the objective of establishing connections between the dormancy status of buds and their effectiveness in vascular water transport. We found large differences in the dormancy status between species throughout the entire investigation period, likely reflecting species-specific environmental requirements to initiate and release dormancy, whereas only small differences in the dormancy status were found between the two studied sites. We found strong 2H-labelled water uptake into buds during leaf senescence, followed by a sharp decrease, which we ascribed to the initiation of endodormancy. However, surprisingly, we did not find a progressive increase in 2H-labelled water uptake into buds as winter advanced. Nonetheless, all examined tree species exhibited a consistent relationship between bud water content and dormancy status. Our results suggest that short-term 2H-labelled water uptake may not be a robust indicator of dormancy release, yet it holds promise as a method for tracking the induction of dormancy in deciduous trees. By contrast, bud water content emerges as a cost-effective and more reliable indicator of dormancy release., (© The Author(s) 2024. Published by Oxford University Press.)

In temperate and boreal regions, perennial plants adapt their annual growth cycle to the change of seasons. In natural forests, juvenile seedlings usually display longer growth seasons compared to adult trees to ensure their establishment and survival under canopy shade. However, how trees adjust their annual growth according to their age is not known. In this study, we show that age-dependent seasonal growth cessation is genetically controlled and found that the miR156-SPL3/5 module, a key regulon of vegetative phase change (VPC), also triggers age-dependent growth cessation in Populus trees. We show that miR156 promotes shoot elongation during vegetative growth, and its targets SPL3/5s function in the same pathway but as repressors. We find that the miR156-SPL3/5s regulon controls growth cessation in both leaves and shoot apices and through multiple pathways, but with a different mechanism compared to how the miR156-SPL regulon controls VPC in annual plants. Taken together, our results reveal an age-dependent genetic network in mediating seasonal growth cessation, a key phenological process in the climate adaptation of perennial trees., Competing Interests: Competing interests statement:The authors declare no competing interest.

The phenological changes induced by climate warming have profound effects on water, energy, and carbon cycling in forest ecosystems. In addition to pre-season warming, growing-season warming may drive tree phenology by altering photosynthetic carbon uptake. It has been reported that the effect of pre-season warming on tree phenology is decreasing. However, temporal change in the effect of growing-season warming on tree phenology is not yet clear. Combining long-term ground observations and remote-sensing data, here we show that spring and autumn phenology were advanced by growing-season warming, while the accelerating effects of growing-season warming on tree phenology were progressively disappearing, manifesting as phenological events converted from being advanced to being delayed, in the temperate deciduous broadleaved forests across the Northern Hemisphere between 1983 and 2014. We further observed that the effect of growing-season warming on photosynthetic productivity showed a synchronized decline over the same period. The responses of phenology and photosynthetic productivity had a strong linear relationship with each other, and both showed significant negative correlations with the elevated temperature and vapor pressure deficit during the growing season. These findings indicate that warming-induced water stress may drive the observed decline in the responses of tree phenology to growing-season warming by decelerating photosynthetic productivity. Our results not only demonstrate a close link between photosynthetic carbon uptake and tree seasonal activities but also provide a physiological perspective of the nonlinear phenological responses to climate warming., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2023 Elsevier Inc. All rights reserved.)

Over the last decades, spring leaf-out of temperate and boreal trees has substantially advanced in response to global warming, affecting terrestrial biogeochemical fluxes and the Earth's climate system. However, it remains unclear whether leaf-out will continue to advance with further warming because species' effective chilling temperatures, as well as the amount of chilling time required to break dormancy, are still largely unknown for most forest tree species. Here, we assessed the progress of winter dormancy and quantified the efficiency of different chilling temperatures in six dominant temperate European tree species by exposing 1170 twig cuttings to a range of temperatures from -2°C to 10°C for 1, 3, 6 or 12 wk. We found that freezing temperatures were most effective for half of the species or as effective as chilling temperatures up to 10°C, that is, leading to minimum thermal time to and maximum success of budburst. Interestingly, chilling duration had a much larger effect on dormancy release than absolute chilling temperature. Our experimental results challenge the common assumption that optimal chilling temperatures range c. 4-6°C, instead revealing strong sensitivity to a large range of temperatures. These findings are valuable for improving phenological models and predicting future spring phenology in a warming world., (© 2021 The Authors New Phytologist © 2021 New Phytologist Foundation.)

Examining whether a phenophase occurrence date in the current year affects the same phenophase occurrence date in the following year is crucial for developing cross-year phenological prediction models. Here, we carried out correlation analyses between leaf unfolding start (LUS)/leaf fall end (LFE) dates in the current and following years for four dominant tree species in temperate northern China from 1981 to 2012. Then, we calculated the recurrence intervals of LUS and LFE between two adjacent years for each species. Moreover, we investigated temperature effects on LUS/LFE dates, growing season and non-growing season lengths. Results show that correlation coefficients between LUS/LFE dates in the current and following years are nonsignificant at most stations. The recurrence interval of a phenophase has slight interannual variation and correlates significantly (and negatively) with the phenophase occurrence date of the current year. Further analyses indicate that LUS dates correlate significantly (and negatively) with spring mean temperatures, while LFE dates correlate significantly (and positively) with autumn mean temperatures, but negatively with growing season mean temperatures. In addition, spring mean temperatures can influence growing season length by controlling LUS date but cannot influence the following non-growing season length. Similarly, autumn mean temperatures and growing season mean temperatures can influence the subsequent non-growing season length but cannot influence the growing season length of the following year. Our study highlights that recurrence interval and time restrictions in the effects of seasonal temperatures on phenophase dates are the main environmental causes of nonsignificant correlations between phenophase occurrence dates in the current and following years.

Regions at high latitudes and high altitudes are undergoing a more pronounced winter warming than spring warming, and such asymmetric warming will affect chilling and forcing processes and thus the spring phenology of plants. We analyzed winter chilling and spring forcing accumulation in relation to the spring phenology of three tree species (Ulmus pumila, Populus simonii, and Syringa oblata) growing in a cold region (CR) compared with trees in a warmer reference region (WR), using the Dynamic Model and the Growing Degree Hour (GDH) model. We tested that forcing rather than chilling affects the spring phenology of trees in CR (hypothesis I), and that trees in CR have both lower mean chilling and forcing temperature and thus longer accumulation periods than trees in WR (hypothesis II). The modeling results confirmed that chilling and forcing occur simultaneously during the early spring when temperature gradually increases. In line with our hypotheses, forcing played a crucial role in spring phenology in CR, but chilling and forcing combined to determine spring phenology in WR. The temperature during the chilling and forcing periods was lower and the accumulation period started earlier and ended later in CR than in WR. Moreover, the chilling accumulation was broken into two periods by the low deep winter temperature in CR, and that interruption will be removed by future strong winter warming. Future asymmetric warming, with a stronger temperature increase in winter than in spring, could decrease the forcing accumulation effects and increase the chilling effects on the spring phenology of plants in CR. This change in the balance between chilling and forcing will lead to a shift in plant phenology, which will further have major impacts on biogeochemical cycles and on ecosystem functions and services., Competing Interests: Declaration of competing interest None., (Copyright © 2020 Elsevier B.V. All rights reserved.)

Extreme climate events (ECEs) such as severe droughts, heat waves, and late spring frosts are rare but exert a paramount role in shaping tree species distributions. The frequency of such ECEs is expected to increase with climate warming, threatening the sustainability of temperate forests. Here, we analyzed 2,844 tree-ring width series of five dominant European tree species from 104 Swiss sites ranging from 400 to 2,200 m a.s.l. for the period 1930-2016. We found that (a) the broadleaved oak and beech are sensitive to late frosts that strongly reduce current year growth; however, tree growth is highly resilient and fully recovers within 2 years; (b) radial growth of the conifers larch and spruce is strongly and enduringly reduced by spring droughts-these species are the least resistant and resilient to droughts; (c) oak, silver fir, and to a lower extent beech, show higher resistance and resilience to spring droughts and seem therefore better adapted to the future climate. Our results allow a robust comparison of the tree growth responses to drought and spring frost across large climatic gradients and provide striking evidence that the growth of some of the most abundant and economically important European tree species will be increasingly limited by climate warming. These results could serve for supporting species selection to maintain the sustainability of forest ecosystem services under the expected increase in ECEs., (© 2019 John Wiley & Sons Ltd.)

13 CO 2 pulse-labelling experiments were performed in situ on adult beeches (Fagus sylvatica) and pines (Pinus pinaster) at different phenological stages to study seasonal and interspecific short-term dynamics and partitioning of recently assimilated carbon (C) in leaves. Polar fraction (PF, including soluble sugars, amino acids and organic acids) and starch were purified from foliage sampled during a 10-d chase period. C contents, isotopic compositions and 13 C dynamics parameters were determined in bulk foliage, PF and starch. Decrease in 13 C amount in bulk foliage followed a two-pool exponential model highlighting 13 C partitioning between 'mobile' and 'stable' pools, the relative proportion of the latter being maximal in beech leaves in May. Early in the growing season, new foliage acted as a strong C sink in both species, but although young leaves and needles were already photosynthesizing, the latter were still supplied with previous-year needle photosynthates 2 months after budburst. Mean 13 C residence times (MRT) were minimal in summer, indicating fast photosynthate export to supply perennial organ growth in both species. In late summer, MRT differed between senescing beech leaves and overwintering pine needles. Seasonal variations of 13 C partitioning and dynamics in field-grown tree foliage are closely linked to phenological differences between deciduous and evergreen trees., (© 2016 The Authors. New Phytologist © 2016 New Phytologist Trust.)

Autumn senescence regulates multiple aspects of ecosystem function, along with associated feedbacks to the climate system. Despite its importance, current understanding of the drivers of senescence is limited, leading to a large spread in predictions of how the timing of senescence, and thus the length of the growing season, will change under future climate conditions. The most commonly held paradigm is that temperature and photoperiod are the primary controls, which suggests a future extension of the autumnal growing season as global temperatures rise. Here, using two decades of ground- and satellite-based observations of temperate deciduous forest phenology, we show that the timing of autumn senescence is correlated with the timing of spring budburst across the entire eastern United States. On a year-to-year basis, an earlier/later spring was associated with an earlier/later autumn senescence, both for individual species and at a regional scale. We use the observed relationship to develop a novel model of autumn phenology. In contrast to current phenology models, this model predicts that the potential response of autumn phenology to future climate change is strongly limited by the impact of climate change on spring phenology. Current models of autumn phenology therefore may overpredict future increases in the length of the growing season, with subsequent impacts for modeling future CO 2 uptake and evapotranspiration., (© 2015 John Wiley & Sons Ltd.)

Recent temperature increases have elicited strong phenological shifts in temperate tree species, with subsequent effects on photosynthesis. Here, we assess the impact of advanced leaf flushing in a winter warming experiment on the current year's senescence and next year's leaf flushing dates in two common tree species: Quercus robur L. and Fagus sylvatica L. Results suggest that earlier leaf flushing translated into earlier senescence, thereby partially offsetting the lengthening of the growing season. Moreover, saplings that were warmed in winter-spring 2009-2010 still exhibited earlier leaf flushing in 2011, even though the saplings had been exposed to similar ambient conditions for almost 1 y. Interestingly, for both species similar trends were found in mature trees using a long-term series of phenological records gathered from various locations in Europe. We hypothesize that this long-term legacy effect is related to an advancement of the endormancy phase (chilling phase) in response to the earlier autumnal senescence. Given the importance of phenology in plant and ecosystem functioning, and the prediction of more frequent extremely warm winters, our observations and postulated underlying mechanisms should be tested in other species.

The impact of global warming on phenology has been widely studied, and almost consistently advancing spring events have been reported. Especially in alpine regions, an extraordinary rapid warming has been observed in the last decades. However, little is known about phenological phases over the whole vegetation period at high elevations. We observed 12 phenological phases of seven tree species and measured air temperature at 42 sites along four transects of about 1000 m elevational range in the years 2010 and 2011 near Garmisch-Partenkirchen, Germany. Site- and species-specific onset dates for the phenological phases were determined and related to elevation, temperature lapse rates and site-specific temperature sums. Increasing temperatures induced advanced spring and delayed autumn phases, in which both yielded similar magnitudes. Delayed leaf senescence could therefore have been underestimated until now in extending the vegetation period. Not only the vegetation period, but also phenological periods extended with increasing temperature. Moreover, sensitivity to elevation and temperature strongly depends on the specific phenological phase. Differences between species and groups of species (deciduous, evergreen, high elevation) were found in onset dates, phenological response rates and also in the effect of chilling and forcing temperatures. Increased chilling days highly reduced forcing temperature requirements for deciduous trees, but less for evergreen trees. The problem of shifted species associations and phenological mismatches due to species-specific responses to increasing temperature is a recent topic in ecological research. Therefore, we consider our findings from this novel, dense observation network in an alpine area of particular importance to deepen knowledge on phenological responses to climate change., (© 2013 German Botanical Society and The Royal Botanical Society of the Netherlands.)