Indirect suppression of photosynthesis on individual leaves by arthropod herbivory

BACKGROUND: Herbivory reduces leaf area, disrupts the function of leaves, and ultimately alters yield and productivity. Herbivore damage to foliage typically is assessed in the field by measuring the amount of leaf tissue removed and disrupted. This approach assumes the remaining tissues are unaltered, and plant photosynthesis and water balance function normally. However, recent application of thermal and fluorescent imaging technologies revealed that alterations to photosynthesis and transpiration propagate into remaining undamaged leaf tissue. SCOPE AND CONCLUSIONS: This review briefly examines the indirect effects of herbivory on photosynthesis, measured by gas exchange or chlorophyll fluorescence, and identifies four mechanisms contributing to the indirect suppression of photosynthesis in remaining leaf tissues: severed vasculature, altered sink demand, defence-induced autotoxicity, and defence-induced down-regulation of photosynthesis. We review the chlorophyll fluorescence and thermal imaging techniques used to gather layers of spatial data and discuss methods for compiling these layers to achieve greater insight into mechanisms contributing to the indirect suppression of photosynthesis. We also elaborate on a few herbivore-induced gene-regulating mechanisms which modulate photosynthesis and discuss the difficult nature of measuring spatial heterogeneity when combining fluorescence imaging and gas exchange technology. Although few studies have characterized herbivore-induced indirect effects on photosynthesis at the leaf level, an emerging literature suggests that the loss of photosynthetic capacity following herbivory may be greater than direct loss of photosynthetic tissues. Depending on the damage guild, ignoring the indirect suppression of photosynthesis by arthropods and other organisms may lead to an underestimate of their physiological and ecological impacts.     

Indirect effects of insect herbivory on leaf gas exchange in soybean

Herbivory can affect plant carbon gain directly by removing photosynthetic leaf tissue and indirectly by inducing the production of costly defensive compounds or disrupting the movement of water and nutrients. The indirect effects of herbivory on carbon and water fluxes of soybean leaves were investigated using gas exchange, chlorophyll fluorescence and thermal imaging. Herbivory by Popillia japonica and Helicoverpa zea (Boddie) caused a 20–90% increase in transpiration from soybean leaflets without affecting carbon assimilation rates or photosynthetic efficiency (Φ_PSII). Mechanical damage to interveinal tissue increased transpiration up to 150%. The spatial pattern of leaf temperature indicated that water loss occurred from injuries to the cuticle as well as from cut edges. A fluorescent tracer (sulforhodamine G) indicated that water evaporated from the apoplast approximately 100 µm away from the cut edges of damaged leaves. The rate of water loss from damaged leaves remained significantly higher than from control leaves for 6 d, during which time they lost 45% more water than control leaves (0.72 mol H₂O per cm of damaged perimeter). Profligate water loss through the perimeter of damaged tissue indicates that herbivory may exacerbate water stress of soybeans under field conditions.     

Photosynthesis and chlorophyllafluorescence during flag leaf senescence of field-grown wheat plants

The characteristics of photosynthetic gas exchange, chlorophyll a fluorescence, and xanthophyll cycle pigments during flag leaf senescence of field-grown wheat plants were investigated. With senescence progressing, the light-saturated net CO₂ assimilation rate expressed either on a basis of leaf area or chlorophyll decreased significantly. The apparent quantum yield of net photosynthesis decreased when expressed on a leaf area basis but increased when expressed on a chlorophyll basis. The maximal efficiency of PSII photochemistry decreased very little while actual PSII efficiency, photochemical quenching, and the efficiency of excitation capture by open PSII centers decreased considerably. At the same time, non-photochemical quenching increased significantly. A substantial decrease in the contents of violaxanthin and zeaxanthin, but a slight decrease in the content of antheraxanthin were observed. However, the de-epoxidation status of the xanthophyll cycle was positively correlated with progressive senescence. This increase was due mainly to a smaller decrease in zeaxanthin than in violaxanthin. Our results suggest that PSII apparatus remained functional, but a down-regulation of PSII occurred under the steady state of photosynthesis in senescent flag leaves. Such a down-regulation was associated with the closure of PSII centers and an enhanced xanthophyll cycle-related thermal dissipation in the PSII antennae.     

基于叶绿素荧光成像及荧光参数分布特征的叶片光合异质性定量分析

植物叶片光合作用具有高度的空间异质性,叶绿素荧光成像技术为叶片光合异质性的研究提供了便利,但叶片光合异质性的定量分析并没有得到广泛应用。本文利用Imaging PAM叶绿素荧光成像系统,获得中亚热带地区越冬期小叶榕(Ficus microcarpa)阳生叶和阴生叶的叶绿素荧光参数图像,并利用仪器的分析软件对其进行分析,定量比较了阳生叶和阴生叶的光合异质性特征。研究发现：越冬期小叶榕阳生叶的光合异质性和光抑制程度明显高于阴生叶,变异系数可作为光合异质性的定量指标。低温强光导致阳生叶坏死率(P_LN)达4.30%,并有53.30%的区域处于严重光抑制(0v/F_m<0.627),但仍有42.27%的区域仅为轻度光抑制(0.627≤F_v/F_m<0.800)。而低温弱光并未造成阴生叶坏死和严重光抑制。通过对光系统Ⅱ(PSⅡ)的实际光合效率(Y(Ⅱ))、调节性能量耗散的量子产额(Y(NPQ))和非调节性能量耗散的量子产额(Y(NO))荧光参数异质性的定量分析表明,阳生叶...     

Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species.

The differential pigment composition and photosynthetic activity of sun and shade leaves of deciduous (Acer pseudoplatanus, Fagus sylvatica, Tilia cordata) and coniferous (Abies alba) trees was comparatively determined by studying the photosynthetic rates via CO(2) measurements and also by imaging the Chl fluorescence decrease ratio (R(Fd)), which is an in vivo indicator of the net CO(2) assimilation rates. The thicker sun leaves and needles in all tree species were characterized by a lower specific leaf area, lower water content, higher total chlorophyll (Chl) a+b and total carotenoid (Cars) content per leaf area unit, as well as higher values for the ratio Chl a/b compared to the much thinner shade leaves and needles that possess a higher Chl a+b and Cars content on a dry matter basis and higher values for the weight ratio Chls/Cars. Sun leaves and needles exhibited higher rates of maximum net photosynthetic CO(2) assimilation (P(Nmax)) measured at saturating irradiance associated with higher maximum stomatal conductance for water vapor efflux. The differences in photosynthetic activity between sun and shade leaves and needles could also be sensed via imaging the Chl fluorescence decrease ratio R(Fd), since it linearly correlated to the P(Nmax) rates at saturating irradiance. Chl fluorescence imaging not only provided the possibility to screen the differences in P(N) rates between sun and shade leaves, but in addition permitted detection and quantification of the large gradients in photosynthetic rates across the leaf area existing in sun and shade leaves.     

Remote sensing of heterogeneity in photosynthetic efficiency, electron transport and dissipation of excess light in Populus deltoides stands under ambient and elevated CO2 concentrations, and in a tropical forest canopy, using a new laser-induced fluorescence transient device

Determining the spatial and temporal diversity of photosynthetic processes in forest canopies presents a challenge to the evaluation of biological feedbacks needed for improvement of carbon and climate models. Limited access with portable instrumentation, especially in the outer canopy, makes remote sensing of these processes a priority in experimental ecosystem and climate change research. Here, we describe the application of a new, active, chlorophyll fluorescence measurement system for remote sensing of light use efficiency, based on analysis of laser‐induced fluorescence transients (LIFT). We used mature stands of Populus grown at ambient (380 ppm) and elevated CO₂ (1220 ppm) in the enclosed agriforests of the Biosphere 2 Laboratory (B2L) to compare parameters of photosynthetic efficiency, photosynthetic electron transport, and dissipation of excess light measured by LIFT and by standard on‐the‐leaf saturating flash methods using a commercially available pulse‐modulated chlorophyll fluorescence instrument (Mini‐PAM). We also used LIFT to observe the diel courses of these parameters in leaves of two tropical forest dominants, Inga and Pterocarpus, growing in the enclosed model tropical forest of B2L. Midcanopy leaves of both trees showed the expected relationships among chlorophyll fluorescence‐derived photosynthetic parameters in response to sun exposure, but, unusually, both displayed an afternoon increase in nonphotochemical quenching in the shade, which was ascribed to reversible inhibition of photosynthesis at high leaf temperatures in the enclosed canopy. Inga generally showed higher rates of photosynthetic electron transport, but greater afternoon reduction in photosynthetic efficiency. The potential for estimation of the contribution of outer canopy photosynthesis to forest CO₂ assimilation, and assessment of its response to environmental stress using remote sensing devices such as LIFT, is briefly discussed.     

Characteristics of gas exchange and chlorophyll fluorescence in red and green leaves of Begonia semperflorens

To determine the effects of leaf colour on gas exchange and chlorophyll fluorescence, two genotypes of Begonia semperflorens with green leaves or red leaves were compared. The red leaves showed a high accumulation of anthocyanins and high absorbance at 282 and 537 nm while the green leaves exhibited a higher net photosynthetic rate and lower thermal dissipation of light energy. It seems likely that anthocyanins in the vacuoles restricted the absorption of green light to the chloroplasts, leading to a decrease in the efficiency of excitation capture by open PS 2 centres, photochemical quenching and CO₂ assimilation.     

Chlorophyll a fluorescence and carbon assimilation in developing leaves of light-grown cucumber

The development of photochemical activity and carbon assimilation in light-grown cucumber (Cucumis sativus L. cv Natsusairaku) leaves was studied to determine the pattern of acquisition and its relationship to leaf growth and expansion. Measurements of chlorophyll a fluorescence showed that leaves acquire photochemical function over a period of 6 or more days, and gas exchange studies showed increases in carbon assimilation over a parallel time period. As leaves expand and mature, they undergo a sequential, three-step series of changes in fluorescence response. The initial kinetics show the absence of wholly functional quenching mechanisms. Dynamic imaging of fluorescence kinetics showed that a temporal series of changes occurred within defined areas of individual developing leaves. The spatial acquisition of photochemical activity in leaves was basipetal as is their directional expansion, development of air spaces and stomata, and the cessation of imported carbon.     

Spatio-temporal heterogeneity in Arabidopsis thaliana leaves under drought stress

Using chlorophyll (chl) fluorescence imaging, we studied the effect of mild (MiDS), moderate (MoDS) and severe (SDS) drought stress on photosystem II (PSII) photochemistry of 4-week-old Arabidopsis thaliana. Spatio-temporal heterogeneity in all chl fluorescence parameters was maintained throughout water stress. After exposure to drought stress, maximum quantum yield of PSII photochemistry (F(v)/F(m)) and quantum efficiency of PSII photochemistry (Φ(PSΙΙ)) decreased less in the proximal (base) than in the distal (tip) leaf. The chl fluorescence parameter F(v) /F(m) decreased less after MoDS than MiDS. Under MoDS, the antioxidant mechanism of A. thaliana leaves seemed to be sufficient in scavenging reactive oxygen species, as evident by the decreased lipid peroxidation, the more excitation energy dissipated by non-photochemical quenching (NPQ) and decreased excitation pressure (1-q(p)). Arabidopsis leaves appear to function normally under MoDS, but do not seem to have particular metabolic tolerance mechanisms under MiDS and SDS, as revealed by the level of lipid peroxidation and decreased quantum yield for dissipation after down-regulation in PSII (Φ(NPQ)), indicating that energy dissipation by down-regulation did not function and electron transport (ETR) was depressed. The simultaneous increased quantum yield of non-regulated energy dissipation (Φ(NO)) indicated that both the photochemical energy conversion and protective regulatory mechanism were insufficient. The non-uniform photosynthetic pattern under drought stress may reflect different zones of leaf anatomy and mesophyll development. The data demonstrate that the effect of different degrees of drought stress on A. thaliana leaves show spatio-temporal heterogeneity, implying that common single time point or single point leaf analyses are inadequate.     

A method for measuring whole plant photosynthesis in Arabidopsis thaliana

Measurement of photosynthesis of intact leaves of Arabidopsis thaliana has been prohibitive due to the small leaf size and prostrate growth habit. Because of the widespread use of Arabidopsis for plant science research it is important to have a procedure for accurate, nondestructive measurement of its photosynthesis. We developed and tested a method for analysis of photosynthesis in whole plants of Arabidopsis. Net carbon assimilation and stomatal conductance were measured with an open gas exchange system and photosynthetic oxygen evolution was determined from chlorophyll fluorescence parameters. Individual plants were grown in 50 cubic centimeter tubes that were attached with an air tight seal to an enclosed gas exchange chamber for measurement of carbon dioxide and water exchange by the whole plant. Chlorophyll fluorescence from intact leaves was simultaneously measured with a pulse modulated fluorometer. Photosynthetic CO₂ assimilation and stomatal conductance rates were calculated with established gas exchange procedures and O₂ evolution was determined from chlorophyll fluorescence measurement of Photosystem II yield. Carbon assimilation and oxygen evolution in response to light intensity and ambient CO₂ concentration was measured and is presented here to demonstrate the potential use of this method for investigation of photosynthesis of Arabidopsis plants in controlled environment conditions.     

O2-dependent inhibition of photosynthetic capacity in intact isolated chloroplasts and isolated cells from spinach leaves illuminated in the absence of CO2

When isolated intact chloroplasts or cells from spinach (Spinacia oleracea L.) leaves are incubated in the light in the absence of CO₂, their capacity for subsequent CO₂-dependent photosynthetic oxygen evolution is drastically decreased. This inhibition is light and oxygen-dependent and can be prevented by addition of bicarbonate. It is concluded that the normal dissipation of photosynthetic energy by carbon assimilation and in processes related to photorespiration is an essential condition for the physiological stability of illuminated intact chloroplasts and cells.Abbreviation chl chlorophyll     

抗旱性不同品种的小麦叶片中光合电子传递和分配对氮素水平的响应

在大田控制条件下,以植物叶片气体交换和叶绿素荧光测定相结合的方法,研究抗旱性不同品种冬小麦拔节期叶片的光合电子传递及激发能利用分配对氮素响应的结果表明,施氮可提高抗旱性不同品种小麦叶片天线色素吸收光能的能力,虽然氮素不能改变激发能在光合碳还原（PCR）和光合碳氧化（PCO）之间的分配比例,但可提高PSⅡ总电子传递速率（JF）和Pn。低氮下不同品种小麦叶片的热耗散比例有差异,但中高氛下叶片之间无显著差异。旱地品种的鼻值随氮素水平的提高而先增加后下降,而水地品种则表现为持续升高：2个小麦品种的叶片J0值随氮素水平的提高而呈持续升高的变化趋势。氮素对叶片PSⅡ反应中心活性有影响．而不同抗旱性品种之间亦有差别,说明施氮可改善小麦叶片热耗散和光化学反应对激发能的竞争关系,从而增强光合机构的自我保护能力。     

Herbivory alters plant carbon assimilation,patterns of biomass allocation and nitrogen use efficiency

Herbivory can trigger physiological processes resulting in leaf and whole plant functional changes. The effects of chronic infestation by an insect on leaf traits related to carbon and nitrogen economy in three Prunus avium cultivars were assessed. Leaves from non-infested trees (control) and damaged leaves from infested trees were selected. The insect larvae produce skeletonization of the leaves leaving relatively intact the vein network of the eaten leaves and the abaxial epidermal tissue. At the leaf level, nitrogen content per mass (N_mass) and per area (N_area), net photosynthesis per mass (A_mass) and per area (A_area), photosynthetic nitrogen-use efficiency (PNUE), leaf mass per area (LMA) and total leaf phenols content were measured in the three cultivars. All cultivars responded to herbivory in a similar fashion. The N_mass, A_mass, and PNUE decreased, while LMA and total content of phenols increased in partially damaged leaves. Increases in herbivore pressure resulted in lower leaf size and total leaf area per plant across cultivars. Despite this, stem cumulative growth tended to increase in infected plants suggesting a change in the patterns of biomass allocation and in resources sequestration elicited by herbivory. A larger N investment in defenses instead of photosynthetic structures may explain the lower PNUE and A_mass observed in damaged leaves. Some physiological changes due to herbivory partially compensate for the cost of leaf removal buffering the carbon economy at the whole plant level.     

D,L-甘油醛处理引起的小麦叶片表观光合量子效率的降低（英文）

D,L-甘油醛(磷酸核酮糖激酶抑制剂,10mmol/L)处理小麦旗叶1 h可降低叶片净光合速率和表观量子效率.同时,光系统Ⅱ光化学效率(△F/Fm′)、电子传递速率(ETR)和单位叶面积ATP含量均降低,而胞间二氧化碳浓度(Ci)和叶绿素荧光非光化学猝灭(NPQ)增加.这些结果说明,D,L-甘油醛引起的小麦旗叶表观量子效率降低是由于光合碳同化受阻对光合电子传递的反馈抑制.     

The study of a determinate growth orchid highlights the role of new leaf production in photosynthetic light acclimation

Plants usually respond to the changes of growth irradiance by a combination of the physiological modifications in their preexisting leaves and the production of new leaves. However, those with a determinate growth habit produce certain number of leaves in a growing season and cannot produce new leaves when light condition changes. We used an epiphytic orchid with only one leaf produced every growing season to examine whether and how determinate growth species adapt to changing environments after their preexisting leaves mature. Leaf photosynthesis and anatomy of Pleione aurita were investigated at full expansion and at 40 days after the fully expanded leaves were transferred from high to low light or from low to high light. Leaves show large physiological and morphological plasticity to light gradients at full expansion and the transferred leaves exhibited multiple physiological modifications, including reallocation of nitrogen between light harvesting and carbon fixation, and enhancement of thermal dissipation in their new environments, to optimize carbon assimilation and avoid photoinhibition. Irrespective of the various changes either to shade or sun, the sole preexisting leaf could not fully acclimate to new light environments due to the mesophyll thickness constraint. This leads to the consequence that only plants exposed to high light throughout the experiment had a positive annual biomass gain. Our results highlighted the importance of new leaf production in the carbon accumulation during photosynthetic light acclimation, and contribute new insights of epiphytes physiological responses to their highly dynamic arboreal habitat.     

基于叶绿素荧光参数的小麦叶片叶绿素相对含量估算方法

叶绿素含量是植物学和农业相关研究领域常用的生理指标.叶绿素含量和叶片光合功能密切相关,但是现有的叶绿素含量的测定方法无法实现叶绿素含量和光合功能的同步测定和关联分析.为解决该问题,本研究通过测定35个小麦品种旗叶的SPAD值和叶绿素荧光诱导动力学曲线,分别使用不同时间的快速叶绿素荧光动力学曲线的荧光值,以及33个常用荧...     

Age-dependent changes in the functions and compositions of photosynthetic complexes in the thylakoid membranes of Arabidopsis thaliana

Photosynthetic complexes in the thylakoid membrane of plant leaves primarily function as energy-harvesting machinery during the growth period. However, leaves undergo developmental and functional transitions along aging and, at the senescence stage, these complexes become major sources for nutrients to be remobilized to other organs such as developing seeds. Here, we investigated age-dependent changes in the functions and compositions of photosynthetic complexes during natural leaf senescence in Arabidopsis thaliana. We found that Chl a/b ratios decreased during the natural leaf senescence along with decrease of the total chlorophyll content. The photosynthetic parameters measured by the chlorophyll fluorescence, photochemical efficiency (F _v/F _m) of photosystem II, non-photochemical quenching, and the electron transfer rate, showed a differential decline in the senescing part of the leaves. The CO₂ assimilation rate and the activity of PSI activity measured from whole senescing leaves remained relatively intact until 28 days of leaf age but declined sharply thereafter. Examination of the behaviors of the individual components in the photosynthetic complex showed that the components on the whole are decreased, but again showed differential decline during leaf senescence. Notably, D1, a PSII reaction center protein, was almost not present but PsaA/B, a PSI reaction center protein is still remained at the senescence stage. Taken together, our results indicate that the compositions and structures of the photosynthetic complexes are differentially utilized at different stages of leaf, but the most dramatic change was observed at the senescence stage, possibly to comply with the physiological states of the senescence process.     

温室栽培对软枣猕猴桃叶片形态及叶绿素荧光特性的影响

【目的】深入研究温室栽培条件下软枣猕猴桃叶片的形态与叶绿素荧光特性,探明温室与露地栽培环境下叶片光形态建成的差异。【方法】以软枣猕猴桃品种‘佳绿’和‘魁绿’的5年生植株为试材,测定温室及露地栽培条件下不同叶龄叶片的叶绿素相对含量及叶绿素荧光参数,分析这些参数在温室与露地栽培条件下的差异。【结果】温室与露地栽培软枣猕猴桃的光形态建成均处于1~40 d叶龄间,不同栽培条件下的同一品种荧光特性趋于一致;花期后,不同栽培条件下的同一品种荧光特性差异较大。温室栽培的软枣猕猴桃叶片叶面积较大,叶绿素b含量较高,趋于阴生叶特性,以吸收光能为基础的性能指数等显著低于露地栽培,对光能的吸收捕获能力较强,但热耗散较高,用于电子传递的能量低于露地栽培,叶绿素荧光参数表现出对环境的适应性变化。【结论】软枣猕猴桃叶片的光形态建成时间为展叶后1~40 d,即在花期之前完成,不同栽培环境无明显差异;温室栽培软枣猕猴桃叶片的光形态建成与露地栽培具显著差异,叶面积明显增大;温室栽培在一定程度上改变了叶片的叶绿素荧光特性,降低了光合性能。     

The Effect of Downy and Powdery Mildew on Grapevine (Vitis vinifera L.) Leaf Gas Exchange

The impact of powdery (Uncinula necator) and downy mildew (Plasmopara viticola) on grapevine leaf gas exchange was analysed. Gas exchange measurements (assimilation A, transpiration E, stomatal conductance g_s, intercellular concentration of CO₂C_i) were made on three different leaf materials: (i) healthy tissue of diseased leaves, (ii) infected tissue of diseased leaves, (iii) healthy tissue of healthy leaves (control treatment). Using the same source of leaf tissue, photosynthetic pigment concentration (chlorophyll a, b) and fluorescence levels (minimal fluorescence F₀, maximal fluorescence F_m and the optimal quantum yield [F_m ? F₀]/F_m) were determined to explain the mechanism of action of the two diseases on leaf assimilation. The results indicated that powdery and downy mildew reduced the assimilation rates, not only through a reduction in green leaf area (visual lesions), but also through an influence on gas exchange of the remaining green leaf tissues, determining a ‘virtual lesion’. The ratios between virtual and visual lesions were higher in powdery mildewed leaves than in the downy mildewed leaves. The photosynthetic fluorescence level (F_v/F_m) was affected by neither of the two pathogens. The reduction in intercellular concentration of CO₂ and photosynthetic pigment may explain the lower assimilation rates in the healthy tissues of powdery and downy mildewed leaves respectively.     

不同剂量^137Cs-γ辐射对毛竹幼苗叶片叶绿素荧光参数的影响

利用不同剂量的137Cs-γ射线对毛竹（Phyllostachys heterocycla ‘Pubescens’）种子进行辐射, 测定实生苗叶片中的光合色素含量和叶绿素荧光参数等指标, 探讨辐射对毛竹幼苗生长的影响, 为筛选有利的突变单株奠定良好基础。结果表明：30或60 Gy的137Cs-γ射线辐射后, 毛竹幼苗的光合色素含量以及最大荧光强度（Fm）、可变荧光强度（Fv）、PSII最大光化学效率（Fv/Fm）、PSII的潜在活性（Fv/Fo）、PSII实际光化学效率（Yield）和表观光合电子传递速率（ETR）等荧光参数值均高于90 Gy辐射处理, 说明较低剂量辐射后PSII反应中心的能量捕获效率高, 且具有较强的光合能力; 而90 Gy的137Cs-γ射线辐射对毛竹的影响则与之相反。不同处理剂量之间叶片光能耗散程度以及表观光合电子传递速率-光合有效辐射（ETR-PAR）响应曲线的分析结果也进一步证实了以上结论。