Photosynthetic acclimation to light gradients in plant stands comes out of shade

Dense plant populations or canopies exhibit a strong enrichment in far-red wavelengths which leads to unequal excitation of the two photosystems. In the long-term plants acclimate to changes in light quality by adjusting photosystem stoichiometry and antenna structure, a mechanism called here long-term response (LTR). Using an artificial light system it is possible to mimic such naturally occurring gradients in light quality under controlled laboratory conditions. By this means we recently demonstrated that the LTR is crucial for plant fitness and survival of Arabidopsis. We could also demonstrate that the chlorophyll fluorescence parameter Fs/Fm is a genuine non-invasive functional indicator for acclimatory changes during the LTR. Here we give supportive data that the Fs/Fm can be also used to monitor the LTR in field experiments in which Arabidopsis plants were grown either under canopies or wavelength-neutral shade. Furthermore our data support the notion that acclimation responses to light quality and light quantity are separate mechanisms. Thus, the long-term response to light quality represents an important and distinct acclimation strategy for improving plant survival under changing light quality conditions.Key words: photosynthetic acclimation, redox control, long-term responses, light quality, Arabidopsis, plant fitness     

Light adaptation/acclimation of photosynthesis and the regulation of ribulose-1,5-bisphosphate carboxylase activity in sun and shade plants

The consequences of light adaptation and acclimation of photosynthesis on photosynthetic nitrogen use efficiency (NUE), particularly as it relates to the efficiency of ribulose-1,5-bisphosphate carboxylase (Rubisco) use in photosynthetic CO₂ assimilation, was studied in the sun species Glycine max and the shade species Alocasia macrorrhiza. Both G. max and A. macrorrhiza were found to possess the capacity for light acclimation of CO₂ assimilation, but over distinctly different ranges of photon flux density (PFD). For each species, light acclimation of photosynthesis had little effect on the rate of photosynthesis per unit Rubisco protein or the light response of Rubisco carbamylation and CA 1P metabolism. In contrast, photosynthesis per unit Rubisco protein was significantly higher in G. max than in A. macrorrhiza, due in part to a lower total (fully carbamylated) molar activity (activity per unit enzyme) of A. macrorrhiza Rubisco than that of G. max. Comparison of the light response of Rubisco regulatory mechanisms between G. max and A. macrorrhiza indicated some degree of adaptation, such that carbamylation was higher and CA 1P levels lower at lower PFDs in the shade species than the sun species. However, this adjustment was not sufficient for Rubisco in low light grown A. macrorrhiza to be fully active at the growth PFD. Photosynthesis in A. macrorrhiza appeared to become RuBP regeneration-limited at lower PFDs than G. max, and this was probably the determinant of the light saturated rate of photosynthesis in the shade species. The low efficiency of Rubisco use in A. macrorrhiza was a major contributing factor to its five- to sixfold lower photosynthetic NUE than G. max. Shade species such as A. macrorrhiza appear to make far from maximal use of Rubisco protein N.     

Photosynthetic acclimation of higher plants to growth in fluctuating light environments

This paper describes a study into the potential of plants to acclimate to light environments that fluctuate over time periods between 15 min and 3 h. Plants of Arabidopsis thaliana (L.) Heynh., Digitalis purpurea L. and Silene dioica (L.) Clairv. were grown at an irradiance 100 mol m^-2 s^-1. After 4–6 weeks, they were transferred to light regimes that fluctuated between 100 and either 475 or 810 mol m^-2 s^-1, in a regular cycle, for 7 days. Plants were shown, in most cases, to be able to undergo photosynthetic acclimation under such conditions, increasing maximum photosynthetic rate. The extent of acclimation varied between species. A more detailed study with S. dioica showed that this acclimation involved changes in both Rubisco protein and cytochrome f content, with only marginal changes in pigment content and composition. Acclimation to fluctuating light, at the protein level, did not fully reflect the acclimation to continuous high light - Rubisco protein increased more than would be expected from the mean irradiance, but less than expected from the high irradiance; cytochrome f increased when neither the mean nor the high irradiance would be expected to induce an increase.This revised version was published online in October 2005 with corrections to the Cover Date.     

Green light for polyphosphoinositide signals in plants

Plant genomes lack homologues of the inositol 1,4,5-trisphosphate receptor and protein kinase C, which are important components of the canonical phospholipase C signalling system in animals. Instead, plants seem to utilize alternative downstream signalling molecules, that is, InsP(6) and phosphatidic acid. Inositol lipids may also function as second messengers themselves. By reversible phosphorylation of the inositol headgroup, five biologically active plant polyphosphoinositides can be detected. Protein targets interact with specific polyphosphoinositide isomers via selective lipid-binding domains, thereby altering their intracellular localization and/or enzymatic activity. Such lipid-binding domains have also been used to create GFP based-lipid biosensors to visualize PPIs dynamics in vivo. Here, we highlight some recent advances and ideas on PPIs' role in plant signalling.     

Photosynthetic acclimation to variability in the light environment of early and late successional plants

Summary Fourteen plant species from early-, mid-, and late-successional habitats were grown for a period of 25 to 50 days in each of two light environments, i.e. full sunlight and in deep shade. The rate of photosynthesis for newly formed leaves was measured as a function of light intensity for plants from each light environment. Photosynthetic flexibility, measured as the difference in response between sun- and shade-grown plants, was determined for each of 5 parameters including dark respiration, quantum yield, light compensation, half-saturating irradiance for photosynthesis, and the photosynthetic rate at 1,400 E m^-2 s^-1. We found photosynthetic flexibility to be high for early successional annuals, intermediate for midsuccessional species, and low for late successional species.     

Hydraulic acclimation to shading in boreal conifers of varying shade tolerance

The purpose of this study was to determine how shading affects the hydraulic and wood‐anatomical characteristics of four boreal conifers (Pinus banksiana, Pinus contorta, Picea glauca and Picea mariana) that differ in shade tolerance. Plants were grown in an open field and under a deciduous‐dominated overstory for 6 years. Sapwood‐ and leaf‐area specific conductivity, vulnerability curves, and anatomical measurements (light and scanning electron microscopy) were made on leading shoots from six to nine trees of each treatment combination. There was no difference in sapwood‐area specific conductivity between open‐grown and understory conifers, although two of four species had larger tracheid diameters in the open. Shaded conifers appeared to compensate for small diameter tracheids by changes in pit membrane structure. Scanning electron microscopy revealed that understory conifers had thinner margo strands, greater maximum pore size in the margo, and more torus extensions. All of these trends may contribute to inadequate sealing of the torus. This is supported by the fact that all species showed increased vulnerability to cavitation when grown in the understory. Although evaporative demand in an understory environment is low, a rapid change into fully exposed conditions could be detrimental for shaded conifers.     

Species-specific acclimation to strong shade modifies susceptibility of conifers to photoinhibition

Photoinhibitory processes in the photosynthetic apparatus of the seedlings of Abies alba (Mill.), Picea abies (Karst.), and Pinus mugo (Turra) growing under strong shade (5 % of full solar irradiance) or full irradiance conditions were investigated in winter and spring using chlorophyll a fluorescence techniques. The extent of photoinhibition in needles as indicated by a decrease in maximum quantum yield of PS II photochemistry (F_v/F_m) depended on species, air temperature and acclimation to the light environment. Unexpectedly, shade-tolerant Abies alba was less affected by low-temperature photoinhibition compared to the other species. F_v/F_m recovered with increasing air temperature. During winter, the seedlings of Picea abies growing in shade showed higher F_v/F_m than those from full light. Non-photochemical quenching of fluorescence (NPQ) measured at the same levels of actinic light was higher in needles acclimated to full light except for Abies alba in February. Photosynthetic performance in term of ETR (apparent electron transfer rate) was also higher in full light-acclimated needles. In April, at ambient temperature, recovery of PS II efficiency from the stress induced by illumination with saturating light was faster in the needles of Picea abies than in those of Abies alba. The shade-acclimated needles of Abies alba and Picea abies showed greater down-regulation of PS II induced by high light stress.     

Photosynthesis,photoinhibition and low temperature acclimation in cold tolerant plants

Cold acclimation requires adjustment to a combination of light and low temperature, conditions which are potentially photoinhibitory. The photosynthetic response of plants to low temperature is dependent upon time of exposure and the developmental history of the leaves. Exposure of fully expanded leaves of winter cereals to short-term, low temperature shiftsinhibits whereas low temperature growthstimulates electron transport capacity and carbon assimilation. However, the photosynthetic response to low temperature is clearly species and cultivar dependent. Winter annuals and algae which actively grow and develop at low temperature and moderate irradiance acquire a resistance to irradiance 5- to 6-fold higher than their growth irradiance. Resistance to short-term photoinhibition (hours) in winter cereals is a reflection of the increased capacity to keep Q_A oxidized under high light conditions and low temperature. This is due to an increased capacity for photosynthesis. These characteristics reflect photosynthetic acclimation to low growth temperature and can be used to predict the freezing tolerance of cereals. It is proposed that the enhanced photosynthetic capacity reflects an increased flux of fixed carbon through to sucrose in source tissue as a consequence of the combined effects of increased storage of carbohydrate as fructans in the vacuole of leaf mesophyll cells and an enhanced export to the crown due to its increased sink activity. Long-term exposure (months) of cereals to low temperature photoinhibition indicates that this reduction of photochemical efficiency of PS II represents a stable, long-term down regulation of PS II to match the energy requirements for CO₂ fixation. Thus, photoinhibition in vivo should be viewed as the capacity of plants to adjust photosynthetically to the prevailing environmental conditions rather than a process which necessarily results in damage or injury to plants. Not all cold tolerant, herbaceous annuals use the same mechanism to acquire resistance to photoinhibition. In contrast to annuals and algae, overwintering evergreens become dormant during the cold hardening period and generally remain susceptible to photoinhibition. It is concluded that the photosynthetic response to low temperatures and susceptibility to photoinhibition are consequences of the overwintering strategy of the plant species.     

Light acclimation,retrograde signalling,cell death and immune defences in plants

This review confronts the classical view of plant immune defence and light acclimation with recently published data. Earlier findings have linked plant immune defences to nucleotide‐binding site leucine‐rich repeat (NBS‐LRR)‐dependent recognition of pathogen effectors and to the role of plasma membrane‐localized NADPH‐dependent oxidoreductase (AtRbohD), reactive oxygen species (ROS) and salicylic acid (SA). However, recent results suggest that plant immune defence also depends on the absorption of excessive light energy and photorespiration. Rapid changes in light intensity and quality often cause the absorption of energy, which is in excess of that required for photosynthesis. Such excessive light energy is considered to be a factor triggering photoinhibition and disturbance in ROS/hormonal homeostasis, which leads to cell death in foliar tissues. We highlight here the tight crosstalk between ROS‐ and SA‐dependent pathways leading to light acclimation, and defence responses leading to pathogen resistance. We also show that LESION SIMULATING DISEASE 1 (LSD1) regulates and integrates these processes. Moreover, we discuss the role of plastid–nucleus signal transduction, photorespiration, photoelectrochemical signalling and ‘light memory’ in the regulation of acclimation and immune defence responses. All of these results suggest that plants have evolved a genetic system that simultaneously regulates systemic acquired resistance (SAR), cell death and systemic acquired acclimation (SAA).     

Fertilization and allelopathy modify Pinus halepensis saplings crown acclimation to shade

Pinus halepensis Mill., is a Mediterranean pioneer forest species with shade-intolerant features. The purpose of this study is to better understand how stand fertility and allelopathic properties of adult trees influence shade acclimation of saplings. Crown growth and morphological plasticity were studied under different light, fertilization, and allelopathic conditions in a nursery experiment. We tested whether shade-acclimation capacity increases with fertilization, and is affected by autotoxicity due to pine leachates. We examined stem diameter, and crown characteristics (length, width, shape, and density) in a factorial experiment with two levels for each tested factor: light (full and 20% reduced light), fertilization (low and high rate of NPK fertilizer) and allelopathy (control and allelopathic leachates uptake). In our study, shading induced a significantly higher crown length, width, and surface. Fertilization strongly increased crown length and vertical expended crown shape (the ratio crown length/crown width). Leachates uptake reduced crown length and density, highlighting an autotoxicity phenomenon. We concluded that P. halepensis saplings presented a shade-avoiding syndrome and that the crown shade-acclimation response increased with fertilization but was severely compromised by autotoxicity. We finally discuss the role of fertilization and allelopathy in early P. halepensis acclimation ability.     

Differential leaf expansion can enable hydraulic acclimation to sun and shade

Although leaf size is one of the most responsive plant traits to environmental change, the functional benefits of large versus small leaves remain unclear. We hypothesized that modification of leaf size within species resulting from differences in irradiance can allow leaves to acclimate to different photosynthetic or evaporative conditions while maintaining an efficient balance between hydraulic supply (vein density) and evaporative demand. To test this, we compared the function and anatomy of leaf hydraulic systems in the leaves of a woody angiosperm (Toona ciliata M. Roem.) grown under high and low irradiance in controlled conditions. Our results confirm that in this species, differential leaf expansion regulates the density of veins and stomata such that leaf hydraulic conductance and stomatal conductance remain proportional. A broader sample of field-grown tree species suggested that differences in leaf venation and stomatal traits induced by sun and shade were not regulated by leaf size in all cases. Our results, however, suggest that leaf size plasticity can provide an efficient way for plants to acclimate hydraulic and stomatal conductances to the contrasting evaporative conditions of sun and shade.     

Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature

Photosynthetic organisms respond to strong illumination by activating several photoprotection mechanisms. One of them, non-photochemical quenching (NPQ), consists in the thermal dissipation of energy absorbed in excess. In vascular plants NPQ relies on the activity of PSBS, whereas in the green algae Chlamydomonas reinhardtii it requires a different protein, LHCSR. The moss Physcomitrella patens is the only known organism in which both proteins are present and active in triggering NPQ, making this organism particularly interesting for the characterization of this protection mechanism. We analysed the acclimation of Physcomitrella to high light and low temperature, finding that these conditions induce an increase in NPQ correlated to overexpression of both PSBS and LHCSR. Mutants depleted of PSBS and/or LHCSR showed that modulation of their accumulation indeed determines NPQ amplitude. All mutants with impaired NPQ also showed enhanced photosensitivity when exposed to high light or low temperature, indicating that in this moss the fast-responding NPQ mechanism is also involved in long-term acclimation.     

Chloroplast acclimation to low osmotic potential

Photosynthetic potential of isolated chloroplasts was investigated during in situ water deficits. An eight day stress cycle imposed on spinach plants reduced leaf _w by 0.57MPa, and leaf by 0.50MPa, resulting in partial turgor maintenance during the stress cycle. Pressure/volume curves confirmed the occurrence of osmotic adjustment. Leaf depression was associated with an altered response of chloroplasts to low in vitro. Optimum reaction medium for photosynthesis shifted from –1.04 to –1.57MPa, and low was not as inhibitory to photosynthesis of plastids pre-exposed to stress in situ. These data indicate that chloroplasts acclimate to low external in response to leaf water deficits. This response was still evident four days after a stress cycle ended, but was nearly reversed eight days after stress. Repeated stress cycles in situ did not increase the degree of chloroplast acclimation to low in vitro. Fast dehydration of leaves did not induce this apparent chloroplast acclimation.Abbreviations osmotic potential - _w water potential - PEG polyethylene glycol 8000 - MPa megapascals     

Photosynthetic acclimation to low temperature by western red cedar seedlings

Imposition of low, but above freezing, temperatures resulted in a gradual increase in the cold hardiness of western red cedar seedlings. This was associated with a decrease in the maximum rates of photosynthetic CO₂ fixation and O₂ evolution, and changes in chlorophyll a fluorescence transients which indicated that photoinhibition had occurred. Maximum photosynthetic rates declined approximately 40% during cold hardening. The leaves changed colour from green to red-brown during the hardening process. The colour change was due to the synthesis of large amounts of the carotenoid rhodoxanthin. Lutein levels doubled, while chlorophyll declined slightly. Dehardening resulted in the rapid recovery of photosynthesis to control levels, the rapid disappearance of rhodoxanthin, and the return of lutein levels to control. It is suggested that rhodoxanthin accumulation at low temperature functions to decrease the light intensity reaching the photosynthetic apparatus. The combination of photoinhibition and rhodoxanthin synthesis probably serves to protect the photosynthetic capacity of the seedlings at low temperature.     

植株叶片的光合色素构成对遮阴的响应

叶绿素在植株体内负责光能的吸收、传递和转化, 类胡萝卜素则行使光能捕获和光破坏防御两大功能, 它们在光合作用中起着非常重要的作用。该文综述了几大主要光合色素的分布和功能, 以及不同物种的色素含量和构成差异。阳生植物的叶黄素库较大, 但脱环氧化水平不及阴生植物。黄体素与叶黄素库的比值与植物的耐阴性呈正相关关系。由不同的遮阴源造成的遮阴环境, 光强和光质有很大的差异, 总体来说对植物生长的影响, 建筑物遮阴<阔叶林遮阴<针叶林遮阴。光强的改变可诱导类胡萝卜素的两大循环——叶黄素循环和黄体素循环。由光强诱导的叶绿素含量和叶绿素a/b比值的改变与该物种的耐阴性无关。短时间的遮阴不会对植物的生长造成危害, 叶黄素库的大小不仅与每天接受的光量子有关, 更与光量子在一天的分布有关, 因为光照和温度是协同作用的。光合作用或色素构成是蓝光、红光和远红光共同作用的结果, 不是某一种单色光所能替代的。我们总结了影响植物色素构成的内因和外因, 指出植物主要通过调整光反应中心和捕光天线色素蛋白复合体的比例, 以及两个光系统的比值来调整色素含量和构成以适应不同的光照条件, 提出了现存研究中存在的一些问题, 旨在为今后的相关研究提供建议。     

A functional comparison of acclimation to shade and submergence in two terrestrial plant species

Terrestrial plants experience multiple stresses when they are submerged, caused both by oxygen deficiency due to reduced gas diffusion in water, and by shade due to high turbidity of the floodwater. It has been suggested that responses to submergence are de facto responses to low light intensity. We investigated the extent to which submergence and shade induce similar acclimation responses by comparing two terrestrial Rumex species that differ in their responses to flooding. Our study confirms that there are strong similarities between acclimation responses to shade and submergence. Petiole length, specific leaf area (SLA), chlorophyll parameters and underwater light-compensation points changed at least qualitatively in the same direction. Maximum underwater photosynthesis rate, however, did discriminate between the functionality of the responses, as the acclimation to submergence appeared to be more effective than acclimation to shade at saturating light. We conclude that acclimation to submergence involves more than an increase in SLA to achieve the significant reduction of diffusion resistance for gas exchange between leaves and the water column.     

Photosynthetic acclimation: state transitions and adjustment of photosystem stoichiometry--functional relationships between short-term and long-term light quality acclimation in plants

In dense plant populations, individuals shade each other resulting in a low-light habitat that is enriched in far-red light. This light quality gradient decreases the efficiency of the photosynthetic light reaction as a result of imbalanced excitation of the two photosystems. Plants counteract such conditions by performing acclimation reactions. Two major mechanisms are known to assure efficient photosynthesis: state transitions, which act on a short-term timescale; and a long-term response, which enables the plant to re-adjust photosystem stoichiometry in favour of the rate-limiting photosystem. Both processes start with the perception of the imbalanced photosystem excitation via reduction/oxidation (redox) signals from the photosynthetic electron transport chain. Recent data in Arabidopsis indicate that initialization of the molecular processes in both cases involve the activity of the thylakoid membrane-associated kinase, STN7. Thus, redox-controlled phosphorylation events may not only adjust photosystem antenna structure but may also affect plastid, as well as nuclear, gene expression. Both state transitions and the long-term response have been described mainly in molecular terms, while the physiological relevance concerning plant survival and reproduction has been poorly investigated. Recent studies have shed more light on this topic. Here, we give an overview on the long-term response, its physiological effects, possible mechanisms and its relationship to state transitions as well as to nonphotochemical quenching, another important short-term mechanism that mediates high-light acclimation. Special emphasis is given to the functional roles and potential interactions between the different light acclimation strategies. A working model displays the various responses as an integrated molecular system that helps plants to acclimate to the changing light environment.     

Slowly reversible de-epoxidation of lutein-epoxide in deep shade leaves of a tropical tree legume may 'lock-in' lutein-based photoprotection during acclimation to strong light

The kinetics of response to strong light have been examined in deeply shaded leaves of the tropical tree legume (Inga sp.) which have extraordinarily high levels of the alpha-xanthophyll lutein-epoxide that are co-located in pigment-protein complexes of the photosynthetic apparatus with the beta-xanthophyll violaxanthin. As in other species, rapidly reversible photoprotection (measured as non-photochemical chlorophyll fluorescence quenching) is initiated within the time frame of sun-flecks (minutes), before detectable conversion of violaxanthin to antheraxanthin or zeaxanthin. Photoprotection is stabilized within hours of exposure to strong light by simultaneously engaging the reversible violaxanthin cycle and a slowly reversible conversion of lutein-epoxide to lutein. It is proposed that this lutein 'locks in' a primary mechanism of photoprotection during photoacclimation in this species, converting efficient light-harvesting antennae of the shade plant into potential excitation dissipating centres. It is hypothesized that lutein occupies sites L2 and V1 in light-harvesting chlorophyll protein complexes of photosystem II, facilitating enhanced photoprotection through the superior singlet and/or triplet chlorophyll quenching capacity of lutein.