The Control of Autumn Senescence in European Aspen

The initiation, progression, and natural variation of autumn senescence in European aspen (Populus tremula) was investigated by monitoring chlorophyll degradation in (1) trees growing in natural stands and (2) cloned trees growing in a greenhouse under various light regimes. The main trigger for the initiation of autumn senescence in aspen is the shortening photoperiod, but there was a large degree of variation in the onset of senescence, both within local populations and among trees originating from different populations, where it correlated with the latitude of their respective origins. The variation for onset of senescence with a population was much larger than the variation of bud set. Once started, autumn senescence was accelerated by low temperature and longer nights, and clones that started to senescence late had a faster senescence. Bud set and autumn senescence appeared to be under the control of two independent critical photoperiods, but senescence could not be initiated until a certain time after bud set, suggesting that bud set and growth arrest are important for the trees to acquire competence to respond to the photoperiodic trigger to undergo autumn senescence. A timetable of events related to bud set and autumn senescence is presented.     

Different strategies for photoprotection during autumn senescence in maple and oak

During autumn senescence, plants must disassemble the photosynthetic apparatus as nutrients are remobilized from the leaves. The goal of this study was to examine changes in relative abundance of photosynthetic proteins and pigments throughout autumn senescence in order to understand the mechanisms of photoprotection used during this process. We sampled leaves from two deciduous tree species [sugar maple (Acer saccharum Marsh.) and swamp white oak (Quercus bicolor Willd.)] throughout autumn during 2010 and 2013. Chlorophyll fluorescence was measured, thylakoids were isolated for western blotting with antibodies to individual proteins and pigment content was assessed. Both species retained high photochemical efficiency until late autumn and showed earlier onset of degradation of photosystem I relative to photosystem II. The species differed in the timing and pattern of degradation of individual photosynthetic proteins and pigments. In maple, there were increases in anthocyanins, more rapid degradation of light‐harvesting proteins and enrichment of xanthophyll cycle pigments in late autumn. In oak, light‐harvesting proteins were retained in higher abundance throughout autumn, PsbS levels increased during early autumn and lutein was enriched in late autumn samples. The results suggest that the species differ in strategies for photoprotection during autumn senescence.     

Effect of pollination success on floral longevity in the orchid Calypso bulbosa (Orchidaceae)

The lifespan of an individual flower is often affected by pollination success. Species differ regarding whether male function (pollen removal), female function (pollen deposition), or both trigger floral senescence. We studied senescence in the singleflowered, deceptive orchid Calypso bulbosa by manipulating the degree of male and female reproductive success. We found that deposition of any amount of pollen resulted in dramatic changes in shape and color within 4 d, whereas unmanipulated flowers and those that had had pollinia removed remained unchanged for 8-11 d after treatment. Selection may favor the reproductive function that is less easily satisfied as the trigger for senescence, because a flower that senesces after accomplishment of this function is likely to have already succeeded at the more easily satisfied one. Deceptive (i.e., rewardless) flowers are more likely to satisfy male than female function since the latter requires that a pollinator be fooled twice, first to pick up pollen and second to deposit it. A survey of naturally pollinated Calypso showed that male function, pollinium removal, was more likely to occur than female function, deposition (95% vs. 66% of visited flowers); thus floral senescence in Calypso is triggered by achievement of the function less likely to succeed. Studies of senescence triggers in species in which female function is more likely to be achieved than male are necessary to further test this hypothesis.     

Phytochrome control of short-day-induced bud set in black cottonwood

In trees and other woody perennial plants, short days (SDs) typically induce growth cessation, the initiation of cold acclimation, the formation of a terminal bud and bud dormancy. Phytochrome control of SD-induced bud set was investigated in two northern clones of black cottonwood (Populus trichocarpa Torr. & Gray) by using night breaks with red light (R) and far-red light (FR). For both clones (BC-1 and BC-2), SD-induced bud set was prevented when R night breaks as short as 2 min were given in the middle of the night. When night breaks with 2 min of R were immediately followed by 2 min of FR, substantial reversibility of bud set was observed for BC-1 but not for BC-2. By comparing the effects of the R night breaks on bud set and the length of specific internodes, we determined that the R night breaks influenced internode elongation in two opposing ways. First, the addition of a R night break to the SD treatment prevented the cessation of internode elongation that is associated with bud set. Those internodes that would not have elongated under SDs (and would have been found within the terminal bud) elongated in the R treatment. Second, the R night breaks decreased internode length relative to the long-day (LD) control. In contrast to the clonal differences in reversibility that we observed for bud set, the decrease in internode length (i.e. the second effect of R) was R/FR reversible in both clones. Based on these results, we conclude that internode elongation is influenced by two distinct types of phytochrome-mediated response. The first response is a typical response to photpperiod, whereas the second response is a typical “end-of-day” response to light quality. Our results demonstrate that SD-induced bud set in black cottonwood is controlled by phytochrome but that clonal differences have an important influence on the R/FR reversibility of this response. The availability of an experimental system in which SD-induced bud set is R/FR reversible will be valuable for studying the physiological genetics of photoperiodism in trees.     

Elevated [CO2] and nutrient status modified leaf phenology and growth rhythm of young Populus trichocarpa trees in a 3-year field study

Young individuals of a single clone of black cottonwood, in Iceland, were exposed for 3 years to elevated atmospheric CO₂ concentrations [CO₂] in whole-tree chambers at natural and high nutrient availability. No treatment effects were found at bud break or the start of shoot extension in spring. Autumn phenology was, however, affected both by elevated [CO₂] and changes in nutrient status. The time of annual growth cessation was linearly related to leaf nitrogen concentration, irrespective of CO₂ treatment. At low (natural) nutrient availability, elevated [CO₂] accelerated growth cessation and bud set, which reduced the period of active growth. An earlier and more pronounced leaf senescence and corresponding loss of photosynthetic capacity further decreased carbon acquisition in elevated [CO₂]. The negative [CO₂] effect on duration of shoot extension and leaf senescence existed, but was not as pronounced, when trees grew at higher nutrient availability. Improved nutrient availability extended the shoot extension period and delayed leaf senescence. It is suggested that trees grown in elevated [CO₂] altered their autumn phenology as an effect of a signal similar to that in trees growing at low nutrient availability, i.e. an imbalance between carbon and nitrogen sources. These alterations in autumn phenology may be important when predicting how trees will grow in a future CO₂ environment.     

Induction of leaf senescence in Arabidopsis thaliana by long days through a light-dosage effect

Given the influence of photoperiod on reproductive development and whole-plant senescence in monocarpic plants, one would suspect that leaf senescence in these plants might be under photoperiodic control. In Arabidopsis thaliana , which is monocarpic and also a nonobligate long-day (LD) plant, LDs (16 h, 300 μmol m⁻² s⁻¹) caused leaves to die earlier than did short days (SDs, 10 h). Since leaf longevity was not paralleled by the reproductive development in the present study, the reproductive structures did not seem to be the primary controls of leaf senescence. The LD effect appeared to depend on the amount of light rather than on day length, for leaves given LDs at reduced light intensity (180 μmol m⁻² s⁻¹) lived longer than those in LDs with full light. In addition, the higher light intensity promoted chlorophyll loss and anthocyanin accumulation in LDs. Thus, senescence of these leaves seems to be governed by light dosage rather than photoperiod. Light may play a natural role in promoting the senescence of A. thaliana leaves.     

Effect of frost nights and day and night temperature during dormancy induction on frost hardiness, tolerance to cold storage and bud burst in seedlings of Norway spruce

For trees, the ability to obtain and maintain sufficient levels of frost hardiness in late autumn, winter and spring is crucial. We report that temperatures during dormancy induction influence bud set, frost hardiness, tolerance to cold storage, timing of bud burst and spring frost hardiness in seedlings of Norway spruce (Picea abies (L.) Karst.). Bud set occurred later in 12°C than in 21°C, and later in cool nights (7°C) than in constant temperature. One weekly frost night (−2.5°C) improved frost hardiness. Cool nights reduced frost hardiness early, but improved hardiness later during cold acclimation. Buds and stems were slightly hardier in 21°C than in 12°C, while needles were clearly hardier in 12°C. Cold daytime temperature, cool nights and one weekly frost night improved cold storability (0.7°C). Seedlings receiving high daytime temperatures burst buds later, and were less injured by light frost some days after bud burst.     

Competitive success of southern populations of Betula pendula and Sorbus aucuparia under simulated southern climate experiment in the subarctic

Global warming has been commonly accepted to facilitate species’ range shifts across latitudes. Cross‐latitudinal transplantations support this; many tree species can well adapt to new geographical areas. However, these studies fail to capture species’ adaptations to new light environment because the experiments were not designed to explicitly separate species’ responses to light and temperature. Here we tested reaction norms of tree seedlings in reciprocal transplantations 1,000 km apart from each other at two latitudes (60°N and 69°N). In contrast to past studies, we exposed our experimental plants to same temperature in both sites (temperature of 60°N growing site is recorded to adjust temperature of 69°N site in real time via Internet connection) while light environment (photoperiod, light quality) remained ambient. Shoot elongation and autumn coloration were studied in seedlings of two deciduous trees (Betula pendula and Sorbus aucuparia), which were expected to respond differently to day length. Sorbus as a member of Rosaceae family was assumed to be indifferent to photoperiod, while Betula responds strongly to day length. We hypothesized that (1) southern and northern populations of both species perform differently; (2) southern populations perform better in both sites; (3) autumn phenology of southern populations may delay in the northern site; (4) and Sorbus aucuparia is less dependent on light environment. According to the hypotheses, shoot elongation of northern population was inherently low in both species. An evolutionary consequence of this may be a competitive success of southern populations under warming climate. Southern population of B. pendula was delayed in autumn coloration, but not in growth cessation. Sorbus aucuparia was less responsive to light environment. The results suggest that light provides selection pressure in range shifts, but the response is species dependent.     

Long‐term changes in the impacts of global warming on leaf phenology of four temperate tree species

Contrary to the generally advanced spring leaf unfolding under global warming, the effects of the climate warming on autumn leaf senescence are highly variable with advanced, delayed, and unchanged patterns being all reported. Using one million records of leaf phenology from four dominant temperate species in Europe, we investigated the temperature sensitivities of spring leaf unfolding and autumn leaf senescence (S_T, advanced or delayed days per degree Celsius). The S_T of spring phenology in all of the four examined species showed an increase and decrease during 1951–1980 and 1981–2013, respectively. The decrease in the S_T during 1981–2013 appears to be caused by reduced accumulation of chilling units. As with spring phenology, the S_T of leaf senescence of early successional and exotic species started to decline since 1980. In contrast, for late successional species, the S_T of autumn senescence showed an increase for the entire study period from 1951 to 2013. Moreover, the impacts of rising temperature associated with global warming on spring leaf unfolding were stronger than those on autumn leaf senescence. The timing of leaf senescence was positively correlated with the timing of leaf unfolding during 1951–1980. However, as climate warming continued, the differences in the responses between spring and autumn phenology gradually increased, so that the correlation was no more significant during 1981–2013. Our results further suggest that since 2000, due to the decreased temperature sensitivity of leaf unfolding the length of the growing season has not increased any more. These finding needs to be addressed in vegetation models used for assessing the effects of climate change.     

Within the genome,long telomeres are more informative than short telomeres with respect to fitness components in a long‐lived seabird

Telomeres, DNA‐protein structures at chromosome ends, shorten with age, and telomere length has been linked to age‐related diseases and survival. In vitro studies revealed that the shortest telomeres trigger cell senescence, but whether the shortest telomeres are also the best biomarker of ageing is not known. We measured telomeres in erythrocytes of wild common terns Sterna hirundo using terminal restriction fragment analysis. This yields a distribution of telomere lengths for each sample, and we investigated how different telomere subpopulations (percentiles) varied in their relation to age and fitness proxies. Longer telomeres within a genome lost more base pairs with age and were better predictors of survival than shorter telomeres. Likewise, fitness proxies such as arrival date at the breeding grounds and reproductive success were best predicted by telomere length at the higher percentiles. Our finding that longer telomeres within a genome predict fitness components better than the shorter telomeres indicates that they are a more informative ageing biomarker. This finding contrasts with the fact that cell senescence is triggered by the shortest telomeres. We suggest that this paradox arises, because longer telomeres lose more base pairs per unit time and thus better reflect the various forms of stress that accelerate telomere shortening, and that telomeres primarily function as biomarker because their shortening reflects cumulative effects of various stressors rather than reflecting telomere‐induced cell senescence.     

The full moon as a synchronizer of circa-monthly biological rhythms: Chronobiologic perspectives based on multidisciplinary naturalistic research

Biological rhythmicity is presumed to be an advantageous genetic adaptation of fitness and survival value resulting from evolution of life forms in an environment that varies predictably-in-time during the 24 h, month, and year. The 24 h light/dark cycle is the prime synchronizer of circadian periodicities, and its modulation over the course of the year, in terms of daytime photoperiod length, is a prime synchronizer of circannual periodicities. Circadian and circannual rhythms have been the major research focus of most scientists. Circa-monthly rhythms triggered or synchronized by the 29.5 day lunar cycle of nighttime light intensity, or specifically the light of the full moon, although explored in waterborne and certain other species, have received far less study, perhaps because of associations with ancient mythology and/or an attitude naturalistic studies are of lesser merit than ones that entail molecular mechanisms. In this editorial, we cite our recent discovery through multidisciplinary naturalistic investigation of a highly integrated circadian, circa-monthly, and circannual time structure, synchronized by the natural ambient nyctohemeral, lunar, and annual light cycles, of the Peruvian apple cactus (C. peruvianus) flowering and reproductive processes that occur in close temporal coordination with like rhythms of the honey bee as its pollinator. This finding led us to explore the preservation of this integrated biological time structure, synchronized and/or triggered by environmental light cues and cycles, in the reproduction of other species, including Homo sapiens, and how the artificial light environment of today in which humans reside may be negatively affecting human reproduction efficiency.     

Low night temperature and inhibition of gibberellin biosynthesis override phytochrome action and induce bud set and cold acclimation, but not dormancy in PHYA overexpressors and wild-type of hybrid aspen

Juvenile trees of temperate and boreal regions cease growth and set buds in autumn in response to short day-lengths (SD) detected by phytochrome. Growth cessation and bud set are prerequisites for the development of winter dormancy and full cold hardiness. In this study we show that the SD-requirement for bud set and cold hardening can be overcome in hybrid aspen (Populus tremula L. × tremuloides Michx.) by low night temperature and inhibition of gibberellin (GA) biosynthesis. Bud set and increased cold hardiness were observed under normally non-inductive long day-length (LD) in wild-type plants, when exposed to low night temperature and paclobutrazol. In addition, the effect of PHYA overexpression could be overcome in transgenic plants, producing bud set and cold acclimation by treatment with: SD, low night temperature and paclobutrazol. After cold acclimation, the degree of bud dormancy was lower for wild-type plants prior treated with LD and transgenic plants (overexpressing PHYA), than SD-treated, wild-type plants. Thus, low night temperature in combination with reduced GA content induced bud set and promoted cold hardiness under normally non-inductive photoperiods in hybrid aspen, but was unable to affect development of dormancy. This might suggest separate signalling pathways from phytochrome regulating the induction of cold/cold hardiness and bud dormancy in hybrid aspen or alternatively, there might be one pathway that fails to complete its action in the transgenic and paclobutrazol treated plants.     

Effect of Light Quality (Red:Far-red Ratio) at the Apical Bud of the Main Stolon on Morphogenesis of Trifolium repens L.

A controlled environment experiment investigated whether thered:far-red (R:FR) ratio of light at the apical bud of the mainstolon could alter plant morphogenesis in clonal cuttings ofwhite clover (Trifolium repens L.) The apical bud included theapical meristem, five to six developing leaf primordia withassociated axillary bud primordia and stipules and the firstemerged folded leaf until development was greater than 0·3on the Carlson scale. Three light regimes were imposed on theapical bud by collimating light from R or FR light-emittingdiodes so that the R:FR ratio of light incident at the apicalbud was set at 0·25, 1·6 or 2·1, withoutsignificantly altering photosynthetically active radiation.The effect of these light regimes on white clover seedling growthwas also tested. At a low R:FR ratio seedling hypocotyl and cotyledon lengthswere significantly longer. However, with the cuttings, the lighttreatments did not alter node appearance rate or internode lengthof the main stolon, petiole length, area of leaves or totalshoot dry matter. There was one significant photomorphogeneticresponse in the cuttings, a delay of 0·5 of a phyllochronin the appearance of branches from axillary buds in the lowR:FR ratio treatment relative to the other treatments. Wherebranch appearance was delayed plants had fewer branches. Thisdifference could be ascribed solely to a delay in branch appearanceas there were no significant treatment effects on either theinitiation of axillary bud primordia within the apical bud,the probability of branching or on the rate of growth of branchesafter appearance. Because treatment of the apical bud inducedonly one of the many previously observed responses of whiteclover to a decrease in the R:FR ratio of light, we concludethat other plant organs must also sense the quality of incidentlight.Copyright 1994, 1999 Academic Press White clover, Trifolium repens, apical bud, light quality, red:far-red ratio, light-emitting diode, branching, axillary buds, photomorphogenesis     

Premature leaf senescence 3, encoding a methyltransferase,is required for melatonin biosynthesis in rice

Premature leaf senescence in rice is one of the most common factors affecting the plant's development and yield. Although methyltransferases are involved in diverse biological functions, their roles in rice leaf senescence have not been previously reported. In this study, we identified the premature leaf senescence 3 (pls3) mutant in rice, which led to early leaf senescence and early heading date. Further investigations revealed that premature leaf senescence was triggered by the accumulation of reactive oxygen species. Using physiological analysis, we found that chlorophyll content was reduced in the pls3 mutant leaves, while hydrogen peroxide (H₂O₂) and malondialdehyde levels were elevated. Consistent with these findings, the pls3 mutant exhibited hypersensitivity to exogenous hydrogen peroxide. The expression of other senescence‐associated genes such as Osh36 and RCCR1 was increased in the pls3 mutant. Positional cloning indicated the pls3 phenotype was the result of a mutation in OsMTS1, which encodes an O‐methyltransferase in the melatonin biosynthetic pathway. Functional complementation of OsMTS1 in pls3 completely restored the wild‐type phenotype. We found leaf melatonin content to be dramatically reduced in pls3, and that exogenous application of melatonin recovered the pls3 mutant's leaf senescence phenotype to levels comparable to that of wild‐type rice. Moreover, overexpression of OsMTS1 in the wild‐type plant increased the grain yield by 15.9%. Our results demonstrate that disruption of OsMTS1, which codes for a methyltransferase, can trigger leaf senescence as a result of decreased melatonin production.     

Seasonal variation in daily insolation induces synchronous bud break and flowering in the tropics

In many temperate plants seasonal variation in day length induces flowering at species-specific times each year. Here we report synchronous bud break and flowering of tropical perennials that cannot be explained by seasonal changes in day length. We recorded flushing and flowering of more than 100 tropical trees, succulents and understory herbs over several years. We observed the following phenological patterns throughout the northern Neotropics: wide-ranging trees flush or flower twice a year at the Equator, but annually further north; many trees leaf out in February; in autumn, wide-ranging perennials flower 4 months earlier in Mexico than at the Equator. This latitudinal variation of phenology parallels that of the annual cycle of daily insolation, a function of day length and solar irradiation. Insolation has two annual maxima at the Equator, it rapidly increases in February at all latitudes, and between Mexico and the Equator its maximum shifts from the summer solstice to the autumn equinox. These unique, manifold correlations suggest that throughout the tropics insolation, rather than day length, may control the phenology of many perennials. Our observations significantly extend current knowledge of environmental signals involved in photoperiodic control of plant development.     

Sucrose and Malic Acid as the Compounds Exported to the Apical Bud of Pea following CO(2) Labeling of the Fruit : No Evidence for a Senescence Factor

The G2 line of peas (Pisum sativum L.) displays senescence and death of the apical bud only in long days and in the presence of fruit. As the removal of fruit prevents senescence, one possible mechanism by which fruits induce senescence is that the fruits produce some `senescence factor' under long day conditions, which is then transported to the apical bud. Allowing developing fruits to photosynthesize in the presence of ¹⁴CO₂ results in the recovery of label in the apical bud. In order to determine the chemical nature of this radiolabeled material, fruits of G2 peas, growing under long days, were exposed to ¹⁴CO₂ at the time when the first senescence symptoms start to appear. The radiolabeled material from apical buds was then extracted, purified, and identified. Using HPLC and GC-MS the major labeled compound found in the apical bud following exposure of pea fruits to ¹⁴CO₂ was identified as sucrose, while malic acid was identified as the major ethyl acetate-soluble compound. These compounds accounted for about 73 and 16%, respectively, of the radioactivity in the apical bud. No other compounds were present in significant amounts. As neither of these chemicals is likely to have any kind of senescence effect, we report no evidence for a senescence factor.     

The Role of Abscisic Acid in Senescence of Detached Tobacco Leaves

The role of abscisic acid in the regulation of senescence was investigated in detached tobacco leaves (Nicotiana rustica L.). Leaves senesced in darkness showed a sharp rise in abscisic acid level in the early stage of aging, followed by a rapid decline later. The same trend was found when leaves were aged in light, but the rise in abscisic acid occurred four days later than in darkness. Senescence was slower in light than in darkness, while salt stress accelerated the processes. Leaves treated with kinetin which senesced in light and darkness, did not show an increase in abscisic acid. Application of kinetin led to a transformation from free to bound ABA. These results may indicate that ABA and cytokinin are involved in a trigger mechanism which regulates senescence; the stage at which this trigger is activated determines the rate of senescence.     

Free radicals and senescence

There is a significant body of experimental evidence that a rise in intracellular reactive oxygen species (ROS) contributes to senescence. Here we review experiments where entry into senescence has been evaluated in cells whose intracellular ROS levels have been modulated by growth in either high or low ambient oxygen concentrations, or where the cellular antioxidant status has been perturbed. In addition, we discuss the observations that senescence triggered by oncogene expression also appears to be in part mediated by a rise in ROS levels. Finally, we discuss the emerging evidence that in vivo senescence might also be triggered by a rise in cellular oxidant levels. Although these data tend to support a role for ROS in mediating senescence, significant questions remain as to whether ROS act in a random or specific fashion and what precise oxidant species acts as the potential senescence trigger.     

Quantitative genetics of bud phenology, frost damage, and winter survival in an F2 family of hybrid poplars

We studied the quantitative genetics of bud phenology, fall frost damage, and winter survival in an F₂ family (no. 822) of Populus hybrids derived from a cross between two full-sub F₁ hybrids (P. trichocarpa (Torr. & Gray×P. deltoides Bartr.). Field traits studied included the timing of bud set (BS_F) in Minnesota and Oregon, the timing of bud flush (BF_F) in Oregon, as well as fall frost damage (FD_F) and winter survival (WS_F) in Minnesota. We conclude that Family 822 has substantial genetic variability for all field traits, BS_F and BF_F are under moderate to strong genetic control (H ² _i =0.48–0.80), FD_F and WS_F are under low to moderate genetic control (H ² _i =0.27–0.40), and late bud set is associated with increased frost damage and decreased winter survival. In a warm greenhouse, we measured the timing of bud set and the number of new leaves on trees growing under either an 8-h photoperiod (BS_SD and NL_SD) or a natural photoperiod (NP) from August to December (BS_NP and NL_NP). We found that BS_SD, NL_SD, and NL_NP are under moderate genetic control (H ² _i =0.53–0.70), but the heritability of BS_NP could not be determined because few trees set bud in the warm greenhouse under the NP. By comparing results from the greenhouse experiments with results from the field, we conclude that the genetic correlation between BS_SD and BS_F (0.53–0.60) is relatively modest and that NPs in the fall are relatively ineffective at promoting bud set under warm greenhouse temperatures, although bud set readily occurred in the field. Although, low levels of light pollution in the greenhouse might have affected BS_NP, results from both greenhouse and field experiments suggest that genetic differences in photoperiodic responses play a modest role in explaining genetic differences in the timing of bud set under natural field conditions. Therefore, genetic differences in responses to other environmental factors, such as temperature, deserve greater attention. Received: 11 November 1999 / Accepted: 24 November 1999