Short photoperiod reduces the temperature sensitivity of leaf‐out in saplings of Fagus sylvatica but not in horse chestnut

Leaf phenology is one of the most reliable bioindicators of ongoing global warming in temperate and boreal zones because it is highly sensitive to temperature variation. A large number of studies have reported advanced spring leaf‐out due to global warming, yet the temperature sensitivity of leaf‐out has significantly decreased in temperate deciduous tree species over the past three decades. One of the possible mechanisms is that photoperiod is limiting further advance to protect the leaves against potential damaging frosts. However, the “photoperiod limitation” hypothesis remains poorly investigated and experimentally tested. Here, we conducted a photoperiod‐ and temperature‐manipulation experiment in climate chambers on two common deciduous species in Europe: Fagus sylvatica (European beech, a typically late flushing species) and Aesculus hippocastanum (horse chestnut, a typically early flushing species). In agreement with previous studies, we found that the warming significantly advanced the leaf‐out dates by 4.3 and 3.7 days/°C for beech and horse chestnut saplings, respectively. However, shorter photoperiod significantly reduced the temperature sensitivity of beech only (3.0 days/°C) by substantially increasing the heat requirement to avoid leafing‐out too early. Interestingly, the photoperiod limitation only occurs below a certain daylength (photoperiod threshold) when the warming increased above 4°C for beech trees. In contrast, for chestnut, no photoperiod threshold was found even when the ambient air temperature was warmed by 5°C. Given the species‐specific photoperiod effect on leaf phenology, the sequence of the leaf‐out timing among forest tree species may change under future climate warming conditions. Nonphotoperiodic species may benefit from warmer springs by starting the growing season earlier than photoperiodic sensitive species, modifying forest ecosystem structure and functions, but this photoperiod limitation needs to be further investigated experimentally in numerous species.     

Simulating the onset of spring vegetation growth across the Northern Hemisphere

Changes in the spring onset of vegetation growth in response to climate change can profoundly impact climate–biosphere interactions. Thus, robust simulation of spring onset is essential to accurately predict ecosystem responses and feedback to ongoing climate change. To date, the ability of vegetation phenology models to reproduce spatiotemporal patterns of spring onset at larger scales has not been thoroughly investigated. In this study, we took advantage of phenology observations via remote sensing to calibrate and evaluated six models, including both one‐phase (considering only forcing temperatures) and two‐phase (involving forcing, chilling, and photoperiod) models across the Northern Hemisphere between 1982 and 2012. Overall, we found that the model that integrated the photoperiod effect performed best at capturing spatiotemporal patterns of spring phenology in boreal and temperate forests. By contrast, all of the models performed poorly in simulating the onset of growth in grasslands. These results suggest that the photoperiod plays a role in controlling the onset of growth in most Northern Hemisphere forests, whereas other environmental factors (e.g., precipitation) should be considered when simulating the onset of growth in grasslands. We also found that the one‐phase model performed as well as the two‐phase models in boreal forests, which implies that the chilling requirement is probably fulfilled across most of the boreal zone. Conversely, two‐phase models performed better in temperate forests than the one‐phase model, suggesting that photoperiod and chilling play important roles in these temperate forests. Our results highlight the significance of including chilling and photoperiod effects in models of the spring onset of forest growth at large scales, and indicate that the consideration of additional drivers may be required for grasslands.     

Genetic analysis and identification of a candidate gene associated with in vitro regeneration ability of cucumber

Key message

Candidate genes associated with in vitro regeneration were identified in cucumber.

Abstract

The ability to regenerate shoots or whole plants from differentiated plant tissues is essential for plant transformation. In cucumber (Cucumis sativus L.), regeneration ability varies considerably across accessions, but the genetic mechanism has not yet been demonstrated. In the present study, 148 recombinant inbred lines and a core collection were examined to identify candidate genes involved in cucumber regeneration. Four QTL for cotyledon regeneration that explained 9.7–16.6% of the phenotypic variation in regeneration were identified on cucumber chromosomes 1, 3, and 6. The loci Fcrms1.1 and Fcrms₊1.1 were consistently detected in the same genetic interval on two regeneration media. A genome-wide association study revealed 18 SNPs (??log(p)?>?5) significantly associated with cotyledon regeneration. Three candidate genes in this region were identified. RT-PCR analyses revealed that Csa1G642540 was significantly more highly expressed in genotypes with high cotyledon regeneration rates than in those with low regeneration. The Csa1G642540 CDS driven by its native promoter was transformed into cucumber line 9110Gt; molecular analyses showed that the T-DNA had integrated into the genomes of 8.6% of regenerated plantlets. The seeds from T₀ plants expressing Csa1G642540 were tested for regeneration from cotyledon explants, and the segregate ratio in regeneration frequency is 3:1. The AT3G44110.1, the homologue gene of Csa1G642540 in Arabidopsis, has been reported as PM H⁺-ATPase activity regulation, integrating flowering signals and enlarging meristem function. These results demonstrate that Csa1G642540 might play an important role in regeneration in cucumber and could serve as a selectable marker for regeneration from cotyledons.

     

Strong impacts of daily minimum temperature on the green‐up date and summer greenness of the Tibetan Plateau

Understanding vegetation responses to climate change on the Tibetan Plateau (TP) helps in elucidating the land–atmosphere energy exchange, which affects air mass movement over and around the TP. Although the TP is one of the world's most sensitive regions in terms of climatic warming, little is known about how the vegetation responds. Here, we focus on how spring phenology and summertime greenness respond to the asymmetric warming, that is, stronger warming during nighttime than during daytime. Using both in situ and satellite observations, we found that vegetation green‐up date showed a stronger negative partial correlation with daily minimum temperature (T_min) than with maximum temperature (T_max) before the growing season (‘preseason’ henceforth). Summer vegetation greenness was strongly positively correlated with summer T_min, but negatively with T_max. A 1‐K increase in preseason T_min advanced green‐up date by 4 days (P < 0.05) and in summer enhanced greenness by 3.6% relative to the mean greenness during 2000–2004 (P < 0.01). In contrast, increases in preseason T_max did not advance green‐up date (P > 0.10) and higher summer T_max even reduced greenness by 2.6% K^?1 (P < 0.05). The stimulating effects of increasing T_min were likely caused by reduced low temperature constraints, and the apparent negative effects of higher T_max on greenness were probably due to the accompanying decline in water availability. The dominant enhancing effect of nighttime warming indicates that climatic warming will probably have stronger impact on TP ecosystems than on apparently similar Arctic ecosystems where vegetation is controlled mainly by T_max. Our results are crucial for future improvements of dynamic vegetation models embedded in the Earth System Models which are being used to describe the behavior of the Asian monsoon. The results are significant because the state of the vegetation on the TP plays an important role in steering the monsoon.     

Phenological responses of Icelandic subarctic grasslands to short‐term and long‐term natural soil warming

The phenology of vegetation, particularly the length of the growing season (LOS; i.e., the period from greenup to senescence), is highly sensitive to climate change, which could imply potent feedbacks to the climate system, for example, by altering the ecosystem carbon (C) balance. In recent decades, the largest extensions of LOS have been reported at high northern latitudes, but further warming‐induced LOS extensions may be constrained by too short photoperiod or unfulfilled chilling requirements. Here, we studied subarctic grasslands, which cover a vast area and contain large C stocks, but for which LOS changes under further warming are highly uncertain. We measured LOS extensions of Icelandic subarctic grasslands along natural geothermal soil warming gradients of different age (short term, where the measurements started after 5 years of warming and long term, i.e., warmed since ≥50 years) using ground‐level measurements of normalized difference vegetation index. We found that LOS linearly extended with on average 2.1 days per °C soil warming up to the highest soil warming levels (ca. +10°C) and that LOS had the potential to extend at least 1 month. This indicates that the warming impact on LOS in these subarctic grasslands will likely not saturate in the near future. A similar response to short‐ and long‐term warming indicated a strong physiological control of the phenological response of the subarctic grasslands to warming and suggested that genetic adaptations and community changes were likely of minor importance. We conclude that the warming‐driven extension of the LOSs of these subarctic grasslands did not saturate up to +10°C warming, and hence that growing seasons of high‐latitude grasslands are likely to continue lengthening with future warming (unless genetic adaptations or species shifts do occur). This persistence of the warming‐induced extension of LOS has important implications for the C‐sink potential of subarctic grasslands under climate change.     

Climate warming increases spring phenological differences among temperate trees

Climate warming has substantially advanced spring leaf flushing, but winter chilling and photoperiod co‐determine the leaf flushing process in ways that vary among species. As a result, the interspecific differences in spring phenology (IDSP) are expected to change with climate warming, which may, in turn, induce negative or positive ecological consequences. However, the temporal change of IDSP at large spatiotemporal scales remains unclear. In this study, we analyzed long‐term in‐situ observations (1951–2016) of six, coexisting temperate tree species from 305 sites across Central Europe and found that phenological ranking did not change when comparing the rapidly warming period 1984–2016 to the marginally warming period 1951–1983. However, the advance of leaf flushing was significantly larger in early‐flushing species EFS (6.7 ± 0.3 days) than in late‐flushing species LFS (5.9 ± 0.2 days) between the two periods, indicating extended IDSP. This IDSP extension could not be explained by differences in temperature sensitivity between EFS and LFS; however, climatic warming‐induced heat accumulation effects on leaf flushing, which were linked to a greater heat requirement and higher photoperiod sensitivity in LFS, drove the shifts in IDSP. Continued climate warming is expected to further extend IDSP across temperate trees, with associated implications for ecosystem function.     

Plant phenology and global climate change: Current progresses and challenges

Plant phenology, the annually recurring sequence of plant developmental stages, is important for plant functioning and ecosystem services and their biophysical and biogeochemical feedbacks to the climate system. Plant phenology depends on temperature, and the current rapid climate change has revived interest in understanding and modeling the responses of plant phenology to the warming trend and the consequences thereof for ecosystems. Here, we review recent progresses in plant phenology and its interactions with climate change. Focusing on the start (leaf unfolding) and end (leaf coloring) of plant growing seasons, we show that the recent rapid expansion in ground‐ and remote sensing‐ based phenology data acquisition has been highly beneficial and has supported major advances in plant phenology research. Studies using multiple data sources and methods generally agree on the trends of advanced leaf unfolding and delayed leaf coloring due to climate change, yet these trends appear to have decelerated or even reversed in recent years. Our understanding of the mechanisms underlying the plant phenology responses to climate warming is still limited. The interactions between multiple drivers complicate the modeling and prediction of plant phenology changes. Furthermore, changes in plant phenology have important implications for ecosystem carbon cycles and ecosystem feedbacks to climate, yet the quantification of such impacts remains challenging. We suggest that future studies should primarily focus on using new observation tools to improve the understanding of tropical plant phenology, on improving process‐based phenology modeling, and on the scaling of phenology from species to landscape‐level.     

A structural and data-driven approach to engineering a plant cytochrome P450 enzyme

Functional manipulation of biosynthetic enzymes such as cytochrome P450 s(or P450 s) has attracted great interest in metabolic engineering of plant natural products. Cucurbitacins and mogrosides are plant triterpenoids that share the same backbone but display contrasting bioactivities. This structural and functional diversity of the two metabolites can be manipulated by engineering P450 s. However, the functional redesign of P450 s through directed evolution(DE) or structure-guided protein engineering is time consuming and challenging, often because of a lack of high-throughput screening methods and crystal structures of P450 s. In this study, we used an integrated approach combining computational protein design, evolutionary information, and experimental data-driven optimization to alter the substrate specificity of a multifunctional P450(CYP87 D20)from cucumber. After three rounds of iterative design and evaluation of 96 protein variants, CYP87 D20, which is involved in the cucurbitacin C biosynthetic pathway, was successfully transformed into a P450 mono-oxygenase that performs a single specific hydroxylation at C11 of cucurbitadienol. This integrated P450-engineering approach can be further applied to create a de novo pathway to produce mogrol, the precursor of the natural sweetener mogroside, or to alter the structural diversity of plant triterpenoids by functionally manipulating other P450 s.     

Shortened temperature‐relevant period of spring leaf‐out in temperate‐zone trees

Temperature during a particular period prior to spring leaf‐out, the temperature‐relevant period (TRP), is a strong determinant of the leaf‐out date in temperate‐zone trees. Climatic warming has substantially advanced leaf‐out dates in temperate biomes worldwide, but its effect on the beginning and length of the TRP has not yet been explored, despite its direct relevance for phenology modeling. Using 1,551 species–site combinations of long‐term (1951–2016) in situ observations on six tree species (namely, Aesculus hippocastanum, Alnus glutinosa, Betula pendula, Fagus sylvatica, Fraxinus excelsior, and Quercus robur) in central Europe, we found that the advancing leaf‐out was accompanied by a shortening of the TRP. On average across all species and sites, the length of the TRP significantly decreased by 23% (p < .05), from 60 ± 4 days during 1951–1965 to 47 ± 4 days during 2002–2016. Importantly, the average start date of the TRP did not vary significantly over the study period (March 2–5, DOY = 61–64), which could be explained by sufficient chilling over the study period in the regions considered. The advanced leaf‐out date with unchanged beginning of the TRP can be explained by the faster accumulation of the required heat due to climatic warming, which overcompensated for the retarding effect of shortening daylength on bud development. This study shows that climate warming has not yet affected the mean TRP starting date in the study region, implying that phenology modules in global land surface models might be reliable assuming a fixed TRP starting date at least for the temperate central Europe. Field warming experiments do, however, remain necessary to test to what extent the length of TRP will continue to shorten and whether the starting date will remain stable under future climate conditions.