Molecular aspects of leaf senescence

Senescence is the last stage of leaf development and one type of programmed cell death that occurs in plants. The relationships among senescence programs that are induced by a variety of factors have been addressed at a molecular level in recent studies. Furthermore, an overlap between the pathogen-response and senescence programs is beginning to be characterized. The complexity of the senescence program is also evident in studies of senescence-specific gene regulation and the role of photosynthesis and plant hormones in senescence regulation. New molecular-genetic approaches are expected to be useful in unraveling the molecular mechanisms of the leaf senescence program.     

Signal transduction in leaf senescence

Leaf senescence is a complex developmental phase that involves both degenerative and nutrient recycling processes. It is characterized by loss of chlorophyll and the degradation of proteins, nucleic acids, lipids, and nutrient remobilization. The onset and progression of leaf senescence are controlled by an array of environmental cues (such as drought, darkness, extreme temperatures, and pathogen attack) and endogenous factors (including age, ethylene, jasmonic acid, salicylic acid, abscisic acid, and cytokinin). This review discusses the major breakthroughs in signal transduction during the onset of leaf senescence, in dark- and drought-mediated leaf senescence, and in various hormones regulating leaf senescence achieved in the past several years. Various signals show different mechanisms of controlling leaf senescence, and cross-talks between different signaling pathways make it more complex. Key senescence regulatory networks still need to be elucidated, including cross-talks and the interaction mechanisms of various environmental signals and internal factors.     

表观遗传调控植物叶片衰老的研究进展

植物叶片衰老是一个非常重要的发育过程,涉及大分子的有序分解从而将营养物质从叶片转移到其他器官,对植物的生存和适应至关重要。叶片衰老主要受植物的发育调控,但同时也受内部和外部环境因素的影响,涉及高度复杂的基因调控网络和多层级的调控。近年来的研究表明表观遗传是调控植物叶片衰老的一种重要调控方式。该研究综述了植物叶片衰老过程中的表观遗传调控机制,包括组蛋白修饰、DNA甲基化、ATP依赖的染色质重塑和非编码RNA介导的调控,并对该领域今后的发展方向进行了展望。     

Identification of early senescence-associated genes in rice flag leaves

Leaf senescence is one of the key stages of plant leaf development. It is a highly complex but ordered process involving expression of large scale senescence associated genes, and its molecular mechanisms still remain unclear. By using suppression subtractive hybridization, 815 ESTs that are up-regulated at the onset of rice flag leaf senescence have been isolated. A total of 533 unigenes have been confirmed by macroarray detection and sequencing. 183 of these unigenes have GO annotations, involved in macromolecule metabolism, protein biosynthesis regulation, energy metabolism, gene expression regulations, detoxification, pathogenicity and stress, cytoskeleton organization and flower development. Another 121 unigenes co-localized with previously reported known stay-green QTLS. RT-PCR analysis on the other novel genes indicated that they can be up-regulated in natural early senescence and induced by hormone. Our results indicate that senescence is closely related to various metabolic pathways, thus providing new insight into the onset of leaf senescence mechanism. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

中国北方树木秋季物候的过程模拟及其区域分异归因

揭示温带落叶树木秋季物候的发生机理对提高生态系统固碳量和植被生产力的预估精度具有重要意义。该研究利用低温和光周期乘积模型模拟了1981-2014年中国北方温带90余个站点6个树种的叶始变色期和落叶末期, 并对逐站点-物种的最优模型进行了模拟精度评价, 分析了最优模型模拟精度的时空差异及其随水分梯度的空间变化。主要结果如下: (1)在诱导叶片衰老方面, 光周期缩短的影响通常大于温度降低的影响。据此建立的叶始变色期和落叶末期最优模型模拟的平均均方根误差分别为6.9 d和6.0 d, 模拟与观测时间序列呈显著正相关关系的比例分别为71.4%和83.6%; (2)最优模型对区域平均和多年平均叶始变色期和落叶末期模拟的绝对误差小于2.4 d, 但模拟日期的时空变幅通常小于观测日期, 这与秋季物候发生日期的高度时间变异性密切相关; (3)水分条件在一定程度上影响叶片衰老诱导途径的选择, 表现为光周期缩短诱导叶片衰老的叶始变色期最优模型所占比例在干旱和半干旱区大于湿润和半湿润区, 而最优模型的模拟精度在湿润和半湿润区高于干旱和半干旱区。该研究验证了低温和光周期乘积模型在中国温带地区的适用性, 并揭示了水分条件对秋季物候发生机理和模拟精度的影响。     

Photo- and antioxidant protection and salicylic acid accumulation during post-anthesis leaf senescence in Salvia lanigera grown under Mediterranean climate

Post-anthesis leaf senescence is a key developmental process in the life of plants as it is the time during which material built up by the plant during its growth phase is mobilized into reproductive tissues. Here we aimed to study the extent of photo- and antioxidant protection and salicylic acid (SA) accumulation during post-anthesis leaf senescence in a perennial plant, Salvia lanigera Poir. grown under Mediterranean field conditions. SA levels increased sharply (up to 2.7-fold) during early stages of leaf senescence until fruit and seed formation occurred (i.e. 4 weeks after anthesis). Later on, SA levels kept at constant high levels until leaf abscission occurred (i.e. 7 weeks after anthesis). Reductions in chlorophyll and carotenoid (lutein, violaxanthin and β-carotene) levels occurred progressively during leaf senescence. In contrast, xanthophyll cycle de-epoxidation increased during early stages of leaf senescence and remained constant later, similar to SA accumulation. Indeed, xanthophyll cycle de-epoxidation strongly positively correlated with SA levels (r² = 0.92). The maximum efficiency of PSII (F_v/F_m ratio) kept around 0.80 throughout the experiment, except during the latest stage of leaf senescence (i.e. after fruit and seed formation), when this ratio decreased to 0.72, thus indicating damage to PSII. It is concluded that endogenous SA levels increase sharply during early stages of post-anthesis leaf senescence and concomitantly with activation of photoprotection mechanisms, such as xanthophyll cycle-dependent excess energy dissipation, thus avoiding damage to PSII until fruit and seed formation have been accomplished.     

Changes in autumn senescence in northern hemisphere deciduous trees: a meta-analysis of autumn phenology studies

Background and Aims Many individual studies have shown that the timing of leaf senescence in boreal and temperate deciduous forests in the northern hemisphere is influenced by rising temperatures, but there is limited consensus on the magnitude, direction and spatial extent of this relationship.Methods A meta-analysis was conducted of published studies from the peer-reviewed literature that reported autumn senescence dates for deciduous trees in the northern hemisphere, encompassing 64 publications with observations ranging from 1931 to 2010.Key Results Among the meteorological measurements examined, October temperatures were the strongest predictors of date of senescence, followed by cooling degree-days, latitude, photoperiod and, lastly, total monthly precipitation, although the strength of the relationships differed between high- and low-latitude sites. Autumn leaf senescence has been significantly more delayed at low (25° to 49°N) than high (50° to 70°N) latitudes across the northern hemisphere, with senescence across high-latitude sites more sensitive to the effects of photoperiod and low-latitude sites more sensitive to the effects of temperature. Delays in leaf senescence over time were stronger in North America compared with Europe and Asia.Conclusions The results indicate that leaf senescence has been delayed over time and in response to temperature, although low-latitude sites show significantly stronger delays in senescence over time than high-latitude sites. While temperature alone may be a reasonable predictor of the date of leaf senescence when examining a broad suite of sites, it is important to consider that temperature-induced changes in senescence at high-latitude sites are likely to be constrained by the influence of photoperiod. Ecosystem-level differences in the mechanisms that control the timing of leaf senescence may affect both plant community interactions and ecosystem carbon storage as global temperatures increase over the next century.     

Apple BT2 protein negatively regulates jasmonic acid‐triggered leaf senescence by modulating the stability of MYC2 and JAZ2

Jasmonic acid (JA) is shown to induce leaf senescence. However, the underlying molecular mechanism is not well understood, especially in woody plants such as fruit trees. In this study, we are interested in exploring the biological role of MdBT2 in JA‐mediated leaf senescence. We found that MdBT2 played an antagonistic role in MdMYC2‐promoted leaf senescence. Our results revealed that MdBT2 interacted with MdMYC2 and accelerated its ubiquitination degradation, thus negatively regulated MdMYC2‐promoted leaf senescence. In addition, MdBT2 acted as a stabilizing factor to improve the stability of MdJAZ2 through direct interaction, thereby inhibited JA‐mediated leaf senescence. Furthermore, our results also showed that MdBT2 interacted with a subset of JAZ proteins in apple, including MdJAZ1, MdJAZ3, MdJAZ4 and MdJAZ8. Our investigations provide new insight into molecular mechanisms of JA‐modulated leaf senescence. The dynamic JA‐MdBT2‐MdJAZ2‐MdMYC2 regulatory module plays an important role in JA‐modulated leaf senescence.     

ORE9, an F-box protein that regulates leaf senescence in Arabidopsis

Senescence is a sequence of biochemical and physiological events that constitute the final stage of development. The identification of genes that alter senescence has practical value and is helpful in revealing pathways that influence senescence. However, the genetic mechanisms of senescence are largely unknown. The leaf of the oresara9 (ore9) mutant of Arabidopsis exhibits increased longevity during age-dependent natural senescence by delaying the onset of various senescence symptoms. It also displays delayed senescence symptoms during hormone-modulated senescence. Map-based cloning of ORE9 identified a 693-amino acid polypeptide containing an F-box motif and 18 leucine-rich repeats. The F-box motif of ORE9 interacts with ASK1 (Arabidopsis Skp1-like 1), a component of the plant SCF complex. These results suggest that ORE9 functions to limit leaf longevity by removing, through ubiquitin-dependent proteolysis, target proteins that are required to delay the leaf senescence program in Arabidopsis.     

Gibberellin and phytochrome control senescence in alstroemeria leaves independently

In alstroemeria ( Alstroemeria hybrida ), leaf senescence is effectively retarded by the application of gibberellins and by low fluences of red light. In this study we examined the possible interaction of gibberellins and red light in the regulation of senescence. Determination of endogenous gibberellins revealed that leaf senescence is accompanied by significant changes in the concentrations of non‐ 13‐hydroxylated gibberellins, the onset of senescence coinciding with a dramatic drop in GA₄, whereas concentrations of 13‐hydroxylated gibberellins are far less influenced. However, no direct effect of red light on a specific GA‐metabolic step could be determined. When exogenously applied, non‐13‐hydroxylated GAs were more active than the 13‐hydroxylated GAs. It appeared that the effect of red light is additive to that of active GAs. We hypothesise that GA₄ and phytochrome control senescence in alstroemeria mainly through separate mechanisms and have independent effects and that the observed differences in gibberellin concentrations are a consequence of delayed leaf senescence rather than a cause for it.     

Large-scale identification of leaf senescence-associated genes

Leaf senescence is a form of programmed cell death, and is believed to involve preferential expression of a specific set of "senescence-associated genes" (SAGs). To decipher the molecular mechanisms and the predicted complex network of regulatory pathways involved in the senescence program, we have carried out a large-scale gene identification study in a reference plant, Arabidopsis thaliana. Using suppression subtractive hybridization, we isolated approximately 800 cDNA clones representing SAGs expressed in senescing leaves. Differential expression was confirmed by Northern blot analysis for 130 non-redundant genes. Over 70 of the identified genes have not previously been shown to participate in the senescence process. SAG-encoded proteins are likely to participate in macromolecule degradation, detoxification of oxidative metabolites, induction of defense mechanisms, and signaling and regulatory events. Temporal expression profiles of selected genes displayed several distinct patterns, from expression at a very early stage, to the terminal phase of the senescence syndrome. Expression of some of the novel SAGs, in response to age, leaf detachment, darkness, and ethylene and cytokinin treatment was compared. The large repertoire of SAGs identified here provides global insights about regulatory, biochemical and cellular events occurring during leaf senescence.     

The impact of photosynthesis on initiation of leaf senescence

Senescence is the last stage of leaf development preceding the death of the organ, and it is important for nutrient remobilization and for feeding sink tissues. There are many reports on leaf senescence, but the mechanisms initiating leaf senescence are still poorly understood. Leaf senescence is affected by many environmental factors and seems to vary in different species and even varieties of plants, which makes it difficult to generalize the mechanism. Here, we give an overview on studies reporting about alterations in the composition of the photosynthetic electron transport chain in chloroplasts during senescence. We hypothesize that alternative electron flow and related generation of the proton motive force required for ATP synthesis become increasingly important during progression of senescence. We address the generation of reactive oxygen species (ROS) in chloroplasts in the initiation of senescence, retrograde signaling from the chloroplast to the nucleus and ROS‐dependent signaling associated with leaf senescence. Finally, a few ideas for increasing crop yields by increasing the chloroplast lifespan are presented.     

Senescence mechanisms induced by phloem girdling in Karelinia caspia

AimsSenescence constitutes the final stage of a plant’s organ and tissue development, and is subject to gene control and strict regulation. Plant senescence is largely influenced by carbohydrate content and phloem girdling can induce leaf senescence. Our general objective is to study the effect of stem girdling on physiological conditions in Karelinia caspia. Specifically, we want to know the senescence processes after phloem girdling. In addition, we also want to know the possible mechanisms for the senescence processes. MethodsThree different types of girdling treatments, normal branch, semi-girdling, and full-girdling were performed on K. caspia. Twenty days after girdling, photosynthetic pigments content, photosynthetic rate, soluble sugar content, starch content, abscisic acid (ABA) content, and leaf water potential were measured.Important findings Phloem girdling can largely induce leaf senescence in K. caspia, and the reasons for leaf senescence may be as follows: girdling resulted in carbohydrate accumulation in leaf which subsequently led to “carbon feast” induced leaf senescence; girdling caused ABA accumulation in leaf and then resulted in senescence; girdling decreased water status, which may be another reason for leaf senescence. Compared with natural senescence, girdling induced senescence was a disorder and disorganized process, only a limited physiological process can be controlled by senescence related gene in the girdling induced senescence process. The most important role for carotenoids in the senescence process is to protect the photosynthetic apparatus from being damaged by excess light and reactive oxygen species. Many physiological indicators declined in the semi-girdled K. caspia leaves just like full-girdled leaves, indicating that portion (e.g. half) of the phloem cannot undertake the transport flux which was done by the whole phloem sieve.     

韧皮部环割诱导下的花花柴衰老机制

衰老是植物器官和组织发育的最后阶段, 是一个受到严格控制的高度协调过程, 其中碳水化合物浓度对衰老的影响十分显著。花花柴(Karelinia caspia)是塔克拉玛干沙漠南缘策勒绿洲的主要植物种, 为了研究花花柴在韧皮部环割后的碳水化合物变化和叶片衰老过程, 对其进行韧皮部环割, 测量叶片光合色素含量、光合速率、可溶性糖含量、淀粉含量、脱落酸(ABA)含量和叶水势。结果表明: (1)环割能够诱导花花柴叶片的衰老, 而诱导叶片衰老的主要因素有: 叶片碳水化合物的积累、叶片ABA含量的上升, 以及叶片水分状况的恶化。(2)相比于自然衰老, 环割诱导的衰老导致许多正常的生理过程受到破坏。(3)类胡萝卜素在衰老过程中主要起光保护的作用。(4)韧皮部半环割也导致花花柴各种生理指标显著下降, 表明植物无法通过增加剩余部分韧皮部筛管的运输通量而达到维持整个韧皮部运输系统顺畅的目的。