Metabolic regulation of leaf senescence: interactions of sugar signalling with biotic and abiotic stress responses

Sugars are important signals in the regulation of plant metabolism and development. During stress and in senescing leaves, sugars often accumulate. In addition, both sugar accumulation and stress can induce leaf senescence. Infection by bacterial and fungal pathogens and attack by herbivores and gall-forming insects may influence leaf senescence via modulation of the sugar status, either by directly affecting primary carbon metabolism or by regulating steady state levels of plant hormones. Many types of biotic interactions involve the induction of extracellular invertase as the key enzyme of an apoplasmic phloem unloading pathway, resulting in a sourcesink transition and an increased hexose/sucrose ratio. Induction of the levels of the phytohormones ethylene and jasmonate in biotic interactions results in accelerated senescence, whereas an increase in plant- or pathogen-derived cytokinins delays senescence and results in the formation of green islands within senescing leaves. Interactions between sugar and hormone signalling also play a role in response to abiotic stress. For example, interactions between sugar and abscisic acid (ABA) signalling may be responsible for the induction of senescence during drought stress. Cold treatment, on the other hand, can result in delayed senescence, despite sugar and ABA accumulation. Moreover, natural variation can be found in senescence regulation by sugars and in response to stress: in response to drought stress, both drought escape and dehydration avoidance strategies have been described in different Arabidopsis accessions. The regulation of senescence by sugars may be key to these different strategies in response to stress.     

Leaf senescence in response to elevated atmospheric CO<Subscript>2</Subscript> concentration and low nitrogen supply

This review reports the physiological and metabolic changes in plants during development under elevated atmospheric carbon dioxide concentration and/or limited-nitrogen supply in order to establish their effects on leaf senescence induction. Elevated CO₂ concentration and nitrogen supply modify gene expression, protein content and composition, various aspects of photosynthesis, sugar metabolism, nitrogen metabolism, and redox state in plants. Elevated CO₂ usually causes sugar accumulation and decreased nitrogen content in plant leaves, leading to imbalanced C/N ratio in mature leaves, which is one of the main factors behind premature senescence in leaves. Elevated CO₂ and low nitrogen decrease activities of some antioxidant enzymes and thus increase H₂O₂ production. These changes lead to oxidative stress that results in the degradation of photosynthetic pigments and eventually induce senescence. However, this accelerated leaf senescence under conditions of elevated CO₂ and limited nitrogen can mobilize nutrients to growing organs and thus ensure their functionality.     

Carbon/Nitrogen Imbalance Associated with Drought-Induced Leaf Senescence in Sorghum bicolor

Drought stress triggers mature leaf senescence, which supports plant survival and remobilization of nutrients; yet leaf senescence also critically decreases post-drought crop yield. Drought generally results in carbon/nitrogen imbalance, which is reflected in the increased carbon:nitrogen (C:N) ratio in mature leaves, and which has been shown to be involved in inducing leaf senescence under normal growth conditions. Yet the involvement of the carbon/nitrogen balance in regulation of drought-induced leaf senescence is unclear. To investigate the role of carbon/nitrogen balance in drought-induced senescence, sorghum seedlings were subjected to a gradual soil drought treatment. Leaf senescence symptoms and the C:N ratio, which was indicated by the ratio of non-structural carbohydrate to total N content, were monitored during drought progression. In this study, leaf senescence developed about 12 days after the start of drought treatment, as indicated by various senescence symptoms including decreasing photosynthesis, photosystem II photochemistry efficiency (Fv/Fm) and chlorophyll content, and by the differential expression of senescence marker genes. The C:N ratio was significantly enhanced 10 to 12 days into drought treatment. Leaf senescence occurred in the older (lower) leaves, which had higher C:N ratios, but not in the younger (upper) leaves, which had lower C:N ratios. In addition, a detached leaf assay was conducted to investigate the effect of carbon/nitrogen availability on drought-induced senescence. Exogenous application of excess sugar combined with limited nitrogen promoted drought-induced leaf senescence. Thus our results suggest that the carbon/nitrogen balance may be involved in the regulation of drought-induced leaf senescence.     

Natural developmental variations in leaf and plant senescence in Arabidopsis thaliana

Leaf senescence is a developmentally regulated process that contributes to nutrient redistribution during reproductive growth and finally leads to tissue death. Manipulating leaf senescence through breeding or genetic engineering may help to improve important agronomic traits, such as crop yield and the storage life of harvested organs. Here, we studied natural variations in the regulation of plant senescence among 16 Arabidopsis thaliana accessions. Chlorophyll content and the proportion of yellow leaves were used as indicator parameters to determine leaf and plant senescence respectively. Our study indicated significant genotype effects on the onset and development of senescence. We selected three late- and five early-senescence accessions for further physiological studies. The relationship between leaf and plant senescence was accession-dependent. There was a significant correlation between plant senescence and the total number of leaves, siliques and plant bolting age. We monitored expression of two senescence marker genes, SAG12 and WRKY53 , to evaluate progression of senescence. Our data revealed that chlorophyll content does not fully reflect leaf age, because even fully green leaves had already commenced senescence at the molecular level. Integrating senescence parameters, such as the proportion of senescent leaves, at the whole plant level provided a better indication of the molecular status of the plant than single leaf senescence parameters.     

低氮诱导玉米幼苗叶片衰老过程中碳氮平衡的动态变化

叶片适时衰老对保证玉米产量有重要意义。本试验以玉米自交系PH6WC和PH4CV为研究对象,通过水培方法,设置低氮(0.04 mmol·L^-1,LN)和正常(4 mmol·L^-1,CK)氮素水平两种处理,在培养2、4、6和8 d后,对其幼苗第2和第3叶片表型、光合特性、叶片中氮素和糖分含量及碳氮比进行分析,旨在探究低氮胁迫下玉米幼苗叶片衰老过程中碳氮平衡的动态变化。结果表明: 与CK相比,LN造成两玉米自交系幼苗第2和第3叶片的面积、生物量、相对叶绿素含量、净光合速率、可溶性糖和淀粉含量均下降,而其氮物质生产能力均先后增加,但第2叶片的变化时间均早于第3叶片;在两叶片的各性状上,均为LN下PH6WC的变化幅度大于PH4CV,且仅幼苗叶片中的碳氮比在LN下显著提高;PH6WC的叶片衰老更快,PH4CV有更强的碳氮平衡能力,其叶片衰老相对滞后。综上,低氮会诱导玉米幼苗叶片衰老,高碳氮比具有促进叶片衰老的调控作用,低氮胁迫下幼苗叶片的碳氮平衡能力在两个玉米基因型间存在较大差异。     

The effect of altered sink-source relations on photosynthetic traits and matter transport during the phase of reproductive growth in the annual herb <Emphasis Type="Italic">Chenopodium album</Emphasis>

Annual plants transport a large portion of carbohydrates and nitrogenous compounds from leaves to seeds during the phase of reproductive growth. This study aimed to clarify how reproductive growth affects photosynthetic traits in leaves and matter transport within the plant in the annual herb Chenopodium album L. Plants were grown in pots and either reproductive tissues or axillary leaves were removed at anthesis. Matter transport was evaluated as temporal changes in dry mass (as a substitute of carbohydrates) and nitrogen content of aboveground organs: leaves, axillary leaves, stems and reproductive tissues. Photosynthetic capacity (light-saturated photosynthetic rate under ambient CO₂ concentration), nitrogen, chlorophyll and soluble protein content were followed in the 20^th leaf that was mature at the start of the experiment. Removal of reproductive tissues resulted in accumulation of dry mass in leaves and axillary leaves, and accumulation of nitrogen in stem as nitrogen resorption from leaves and axillary leaves proceeded with time. Removal of axillary leaves proportionally reduced dry mass and nitrogen allocation to reproductive tissues, thus affecting the quantity but not quality of seeds. Removal treatments did not alter the time course of photosynthetic capacity, nitrogen, chlorophyll or soluble protein content during senescence in the 20^th leaf, but changed the photosynthetic capacity per unit of leaf nitrogen according to demand from reproductive tissues. Together, the results indicate that reproductive tissues affected carbon and nitrogen economy separately. The amount of carbon was adjusted in leaves through photosynthetic capacity and carbohydrate export from them, and the amount of nitrogen was adjusted by transport from stem to reproductive tissues. The plant’s ability to independently regulate carbon and nitrogen economy should be important in natural habitats where the plant carbon-nitrogen balance can easily be disturbed by external factors.     

Nitrogen- and storage-affected carbohydrate partitioning in high-light-adapted Pelargonium cuttings in relation to survival and adventitious root formation under low light

BACKGROUND AND AIMS: The aim of this study was to determine the role of nitrogen- and storage-affected carbohydrate availability in rooting of pelargonium cuttings, focusing on the environmental conditions of stock plant cultivation at low latitudes, transport of cuttings, and rooting under the low light that prevails during the winter rooting period in Central European greenhouses. METHODS: Carbohydrate partitioning in high-light-adapted cuttings of the cultivar 'Isabell' was studied in relation to survival and adventitious root formation under low light. Effects of a graduated supply of mineral nitrogen to stock plants and of cutting storage were examined. KEY RESULTS: Nitrogen deficiency raised starch levels in excised cuttings, whereas the concentrations of glucose and total sugars in leaves and the basal stem were positively correlated with internal total nitrogen (Nt). Storage reduced starch to trace levels in all leaves, but sugar levels were only reduced in tissues of non-nitrogen deficient cuttings. Sugars accumulated in the leaf lamina of stored cuttings during the rooting period, whereas carbohydrates were simultaneously exhausted in all other cutting parts including the petioles, thereby promoting leaf senescence. The positive correlation between initial Nt and root number disappeared after storage. Irrespectively of storage, higher pre-rooting leaf glucose promoted subsequent sugar accumulation in the basal stem and final root number. The positive relationships between initial sugar levels in the stems with cutting survival and in leaves with root formation under low light were confirmed in a sample survey with 21 cultivars provided from different sources at low latitudes. CONCLUSIONS: The results indicate that adventitious rooting of pelargonium cuttings can be limited by the initial amount of nitrogen reserves. However, this relationship reveals only small plasticity and is superimposed by a predominant effect of carbohydrate availability that depends on the initial leaf sugar levels, when high-light adaptation and low current light conditions impair net carbon assimilation.     

Leaf canopy as a dynamic system: ecophysiology and optimality in leaf turnover

BACKGROUND AND AIMS: In a leaf canopy, there is a turnover of leaves; i.e. they are produced, senesce and fall. These processes determine the amount of leaf area in the canopy, which in turn determines canopy photosynthesis. The turnover rate of leaves is affected by environmental factors and is different among species. This mini-review discusses factors responsible for leaf dynamics in plant canopies, focusing on the role of nitrogen. SCOPE: Leaf production is supported by canopy photosynthesis that is determined by distribution of light and leaf nitrogen. Leaf nitrogen determines photosynthetic capacity. Nitrogen taken up from roots is allocated to new leaves. When leaves age or their light availability is lowered, part of the leaf nitrogen is resorbed. Resorbed nitrogen is re-utilized in new organs and the rest is lost with dead leaves. The sink-source balance is important in the regulation of leaf senescence. Several models have been proposed to predict response to environmental changes. A mathematical model that incorporated nitrogen use for photosynthesis explained well the variations in leaf lifespan within and between species. CONCLUSION: When leaf turnover is at a steady state, the ratio of biomass production to nitrogen uptake is equal to the ratio of litter fall to nitrogen loss, which is an inverse of the nitrogen concentration in dead leaves. Thus nitrogen concentration in dead leaves (nitrogen resorption proficiency) and nitrogen availability in the soil determine the rate of photosynthesis in the canopy. Dynamics of leaves are regulated so as to maximize carbon gain and resource-use efficiency of the plant.     

Growth under elevated atmospheric CO(2) concentration accelerates leaf senescence in sunflower (Helianthus annuus L.) plants

Some morphogenetic and metabolic processes were sensitive to a high atmospheric CO(2) concentration during sunflower primary leaf ontogeny. Young leaves of sunflower plants growing under elevated CO(2) concentration exhibited increased growth, as reflected by the high specific leaf mass referred to as dry weight in young leaves (16days). The content of photosynthetic pigments decreased with leaf development, especially in plants grown under elevated CO(2) concentrations, suggesting that high CO(2) accelerates chlorophyll degradation, and also possibly leaf senescence. Elevated CO(2) concentration increased the oxidative stress in sunflower plants by increasing H(2)O(2) levels and decreasing activity of antioxidant enzymes such as catalase and ascorbate peroxidase. The loss of plant defenses probably increases the concentration of reactive oxygen species in the chloroplast, decreasing the photosynthetic pigment content as a result. Elevated CO(2) concentration was found to boost photosynthetic CO(2) fixation, especially in young leaves. High CO(2) also increased the starch and soluble sugar contents (glucose and fructose) and the C/N ratio during sunflower primary leaf development. At the beginning of senescence, we observed a strong increase in the hexoses to sucrose ratio that was especially marked at high CO(2) concentration. These results indicate that elevated CO(2) concentration could promote leaf senescence in sunflower plants by affecting the soluble sugar levels, the C/N ratio and the oxidative status during leaf ontogeny. It is likely that systemic signals produced in plants grown with elevated CO(2), lead to early senescence and a higher oxidation state of the cells of these plant leaves.     

Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels?

This review examines the hypotheses that developmental programmed cell death in leaves is mediated (i) by sugar starvation in the leaf cells or (ii) by sugar accumulation in these cells. Experimental evidence for both hypotheses is critically discussed and found to be lacking. For example, some papers show that sugars prevent senescence of cut leaves placed in darkness, and prevent low sugar levels in the leaves. In these tests, the sugars seem to replace photosynthesis, hence the results have little relevance to leaf senescence in intact plants in the light. Low nitrogen nutrition and high light results in earlier senescence than the low nitrogen treatment alone. This is accompanied by high sugar levels in the leaves. The results have led to the idea that accumulation of sugars is the cause of the additional effect, or more generally, that sugar accumulation is always the direct cause of leaf senescence. Results from over-expressing, or knocking out, hexokinase genes tend to support the high sugar hypothesis, but pleiotropic effects confound this conclusion. In addition, several experiments show the effects of treatments on senescence without the increase in leaf sugar levels. Nonetheless, sugar levels are usually measured in whole leaves. Such an overall level does not reflect the differences in the onset of senescence between tissues and cells, and can therefore not be used as an argument for or against either of the two hypotheses. It is argued that future work should determine the time line of the concentrations of various sugars in various cells and cellular compartments, in relation to senescence processes in the same cells. Taken together, the data are not decisive. It is possible that neither of the two hypotheses is correct.     

CO(2) enrichment enhances flag leaf senescence in barley due to greater grain nitrogen sink capacity

Senescence is a highly regulated process which is under genetic control. In monocarpic plants, the onset of fruit development is the most important factor initiating the senescence process. During senescence, a large fraction of plant nutrients is reallocated away from vegetative tissues into generative tissues. Senescence may therefore be regarded as a highly effective salvage mechanism to save nutrients for the offspring. CO(2) enrichment, besides increasing growth and yield of C(3) plants, has often been shown to accelerate leaf senescence. C(3) plants grown under elevated CO(2) experience alterations in their nutrient relations. In particular their tissue nitrogen concentrations are always lower after exposure to elevated CO(2). We used a monocarpic C(3) crop - spring barley (Hordeum vulgare cv. Alexis) - grown in open-top field chambers to test the effects of CO(2) enrichment on growth and yield, on nitrogen acquisition and redistribution, and on the senescence process in flag leaves, at two applications of nitrogen fertilizer. CO(2) enrichment (650 vs. 366 μmol mol(-1)) caused an increase both in biomass and in grain yield by 38% (average of the two fertilizer applications) which was due to increased tillering. Total nitrogen uptake of the crops was not affected by CO(2) treatment but responded solely to the N supply. Nitrogen concentrations in grains and straw were significantly lower (-33 and -24%) in plants grown at elevated CO(2). Phenological development was not altered by CO(2) until anthesis. However, progress of flag leaf senescence as assessed by chlorophyll content, protein content and content of large and small subunit of RubisCO and of cytochrome b559 was enhanced under elevated CO(2) concentrations by approximately 4 days. We postulate that CO(2) enhanced flag leaf senescence in barley crops by increasing the nitrogen sink capacity of the grains.     

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.     

Genome-Wide Association Studies Identify Heavy Metal ATPase3 as the Primary Determinant of Natural Variation in Leaf Cadmium in Arabidopsis thaliana

Understanding the mechanism of cadmium (Cd) accumulation in plants is important to help reduce its potential toxicity to both plants and humans through dietary and environmental exposure. Here, we report on a study to uncover the genetic basis underlying natural variation in Cd accumulation in a world-wide collection of 349 wild collected Arabidopsis thaliana accessions. We identified a 4-fold variation (0.5-2 μg Cd g(-1) dry weight) in leaf Cd accumulation when these accessions were grown in a controlled common garden. By combining genome-wide association mapping, linkage mapping in an experimental F2 population, and transgenic complementation, we reveal that HMA3 is the sole major locus responsible for the variation in leaf Cd accumulation we observe in this diverse population of A. thaliana accessions. Analysis of the predicted amino acid sequence of HMA3 from 149 A. thaliana accessions reveals the existence of 10 major natural protein haplotypes. Association of these haplotypes with leaf Cd accumulation and genetics complementation experiments indicate that 5 of these haplotypes are active and 5 are inactive, and that elevated leaf Cd accumulation is associated with the reduced function of HMA3 caused by a nonsense mutation and polymorphisms that change two specific amino acids.