The genetic architecture of ecophysiological and circadian traits in Brassica rapa

Developmental mechanisms that enable perception of and response to the environment may enhance fitness. Ecophysiological traits typically vary depending on local conditions and contribute to resource acquisition and allocation, yet correlations may limit adaptive trait expression. Notably, photosynthesis and stomatal conductance vary diurnally, and the circadian clock, which is an internal estimate of time that anticipates diurnal light/dark cycles, may synchronize physiological behaviors with environmental conditions. Using recombinant inbred lines of Brassica rapa, we examined the quantitative-genetic architecture of ecophysiological and phenological traits and tested their association with the circadian clock. We also investigated how trait expression differed across treatments that simulated seasonal settings encountered by crops and naturalized populations. Many ecophysiological traits were correlated, and some correlations were consistent with expected biophysical constraints; for example, stomata jointly regulate photosynthesis and transpiration by affecting carbon dioxide and water vapor diffusion across leaf surfaces, and these traits were correlated. Interestingly, some genotypes had unusual combinations of ecophysiological traits, such as high photosynthesis in combination with low stomatal conductance or leaf nitrogen, and selection on these genotypes could provide a mechanism for crop improvement. At the genotypic and QTL level, circadian period was correlated with leaf nitrogen, instantaneous measures of photosynthesis, and stomatal conductance as well as with a long-term proxy (carbon isotope discrimination) for gas exchange, suggesting that gas exchange is partly regulated by the clock and thus synchronized with daily light cycles. The association between circadian rhythms and ecophysiological traits is relevant to crop improvement and adaptive evolution.     

Environmental effects on circadian rhythms in photosynthesis and stomatal opening

Persistent circadian rhythms in photosynthesis and stomatal opening occurred in bean (Phaseolus vulgaris L.) plants transferred from a natural photoperiod to a variety of constant conditions. Photosynthesis, measured as carbon assimilation, and stomatal opening, as conductance to water vapor, oscillated with a freerunning period close to 24 h under constant moderate light, as well as under light-limiting and CO₂-limiting conditions. The rhythms damped under constant conditions conducive to high photosynthetic rates, as did rates of carbon assimilation and stomatal conductance, and this damping correlated with the accumulation of carbohydrate. No rhythm in respiration occurred in plants transferred to constant darkness, and the rhythm in stomatal opening damped rapidly in constant darkness. Damping of rhythms also occurred in leaflets exposed to constant light and CO₂-free air, demonstrating that active photosynthesis and not simply light was necessary for sustained expression of these rhythms. This is CIWDPB Publication No. 1142 This research was supported by National Science Foundation grant BSR 8717422 (C.B.F.) and a U.S. Department of Agriculture training grant to Stanford University (T.L.H.).     

Evidence of multiple circadian oscillators in bean plants.

Circadian rhythms in stomatal opening and photosynthesis had shorter free-running periods than circadian rhythms in leaflet movement in bean plants (Phaseolus vulgaris L.) transferred from 12-hr photoperiods to constant conditions. The rhythm in leaflet movement had a period close to 27 hr, whereas the rhythm in stomatal opening, measured as conductance to water vapor, had a period close to 24 hr. Photosynthesis, measured as net assimilation of CO2, also oscillated with a period close to 24 hr. The periods of these rhythms did not vary with increasing temperature, demonstrating temperature compensation of the controlling oscillators. The difference in free-running periods displayed by these rhythms is evidence that multiple oscillators with different intrinsic frequencies operate in bean plants.     

Circadian Rhythms in Stomatal Responsiveness to Red and Blue Light

Stomata of many plants have circadian rhythms in responsiveness to environmental cues as well as circadian rhythms in aperture. Stomatal responses to red light and blue light are mediated by photosynthetic photoreceptors; responses to blue light are additionally controlled by a specific blue-light photoreceptor. This paper describes circadian rhythmic aspects of stomatal responsiveness to red and blue light in Vicia faba. Plants were exposed to a repeated light:dark regime of 1.5:2.5 h for a total of 48 h, and because the plants could not entrain to this short light:dark cycle, circadian rhythms were able to "free run" as if in continuous light. The rhythm in the stomatal conductance established during the 1.5-h light periods was caused both by a rhythm in sensitivity to light and by a rhythm in the stomatal conductance established during the preceding 2.5-h dark periods. Both rhythms peaked during the middle of the subjective day. Although the stomatal response to blue light is greater than the response to red light at all times of day, there was no discernible difference in period, phase, or amplitude of the rhythm in sensitivity to the two light qualities. We observed no circadian rhythmicity in net carbon assimilation with the 1.5:2.5 h light regime for either red or blue light. In continuous white light, small rhythmic changes in photosynthetic assimilation were observed, but at relatively high light levels, and these appeared to be attributable largely to changes in internal CO2 availability governed by stomatal conductance.     

Genetic variation in circadian regulation of nocturnal stomatal conductance enhances carbon assimilation and growth

Circadian resonance, whereby a plant's endogenous rhythms are tuned to match environmental cues, has been repeatedly shown to be adaptive, although the underlying mechanisms remain elusive. Concomitantly, the adaptive value of nocturnal transpiration in C₃ plants remains unknown because it occurs without carbon assimilation. These seemingly unrelated processes are interconnected because circadian regulation drives temporal patterns in nocturnal stomatal conductance, with maximum values occurring immediately before dawn for many species. We grew individuals of six Eucalyptus camaldulensis genotypes in naturally lit glasshouses and measured sunset, predawn and midday leaf gas exchange and whole‐plant biomass production. We tested whether sunrise anticipation by the circadian clock and subsequent increases in genotype predawn stomatal conductance led to rapid stomatal opening upon illumination, ultimately affecting genotype differences in carbon assimilation and growth. We observed faster stomatal responses to light inputs at sunrise in genotypes with higher predawn stomatal conductance. Moreover, early morning and midday stomatal conductance and carbon assimilation, leaf area and total plant biomass were all positively correlated with predawn stomatal conductance across genotypes. Our results lead to the novel hypothesis that genotypic variation in the circadian‐regulated capacity to anticipate sunrise could be an important factor underlying intraspecific variation in tree growth.     

Circadian Stomatal Rhythms in Epidermal Peels from Vicia faba

Circadian rhythms in stomatal aperture and in stomatal conductance have been observed previously. Here we investigate circadian rhythms in apertures that persist in functionally isolated guard cells in epidermal peels of Vicia faba, and we compare these rhythms with rhythms in stomatal conductance in attached leaves. Functionally isolated guard cells kept in constant light display a rhythmic change in aperture superimposed on a continuous opening trend. The rhythm free-runs with a period of about 22 hours and is temperature compensated between 20 and 30°C. Functionally isolated guard cell pairs are therefore capable of sustaining a true circadian rhythm without interaction with mesophyll cells. Stomatal conductance in whole leaves displays a more robust rhythm, also temperature-compensated, and with a period similar to that observed for the rhythm in stomatal aperture in epidermal peels. When analyzed individually, some stomata in epidermal peels showed a robust rhythm for several days while others showed little rhythmicity or damped out rapidly. Rhythmic periods may vary between individual stomata, and this may lead to desynchronization within the population.     

Sink feedback regulation of photosynthesis in vines: measurements and a model.

An experimental and modelling study of source-sink interactions in Vitis vinifera L., cv. Cabernet Sauvignon, rooted cuttings under non-limiting environmental conditions with a 12 h photoperiod is presented here. After 4 h, measured photosynthesis, stomatal conductance and leaf carbohydrate content reached maximum values. Over the remainder of the photoperiod, photosynthesis and stomatal conductance decreased continuously, whereas leaf carbohydrate content remained relatively constant. Because the experiment took place in a non-limiting environment, the results suggest that stomatal regulation of photosynthesis was mediated by an internal factor, possibly related to sink activity. A simple 1-source, 2-sink model was developed to examine the extent to which the data could be explained by a hypothetical sink-to-source feedback mechanism mediated by carbohydrate levels in either the mesophyll, the source phloem or the phloem of one of the two sinks. Model simulations reproduced the data well under the hypothesis of a phloem-based feedback signal, although the data were insufficient to elucidate the detailed nature of such a signal. In a sensitivity analysis, the steady-state response of photosynthesis to sink activity was explored and predictions made for the partitioning of photosynthate between the two sinks. The analysis highlights the effectiveness of a phloem-based feedback signal in regulating the balance between source and sink activities. However, other mechanisms for the observed decline in photosynthesis, such as photoinhibition, endogenous circadian rhythms or hydraulic signals in the leaf cannot be excluded. Nevertheless, it is concluded that the phloem-based feedback model developed here may provide a useful working hypothesis for incorporation into plant growth models and for further development and testing.     

植物气孔导度的机理模型

Ball-Berry气孔导度模型及其修正模型是评价植物叶片气孔调节的重要工具。该文从CO₂分子在叶片气孔中扩散这个最基本的物理过程出发, 应用物理学中的分子扩散和碰撞理论、流体力学与植物生理学等知识, 严格推导出叶片气孔导度的机理模型。利用美国Li-Cor公司生产的Li-6400光合作用测定仪控制CO₂浓度、湿度和温度, 测量了华北平原冬小麦(Triticum aestivum)的光响应数据和气孔导度数据。拟合结果表明: 推导的气孔导度机理模型较之Ball-Berry气孔导度模型和Tuzet等气孔导度模型, 能更好地描述冬小麦的气孔导度与净光合速率之间的关系。如果用气孔导度的机理模型耦合光合作用对光响应的修正模型, 则耦合模型可以很好地描述华北平原冬小麦叶片气孔导度对光强的响应曲线, 并可直接估算冬小麦的最大气孔导度和对应的饱和光强, 同时可以研究最大气孔导度是否与最大净光合速率同步的问题。拟合结果还表明: 冬小麦在30 ℃、560 μmol·mol^-1CO₂, 或在32 ℃、370 μmol·mol^-1CO₂条件下, 最大气孔导度与最大净光合速率并不同步。     

Development of a photosynthesis model with an emphasis on ecological applications

Summary A physiologically based steady-state model of whole leaf photosynthesis (WHOLEPHOT) is used to describe net photosynthesis daily time courses in Prunus armeniaca. Net photosynthesis rates are calculated in response to incident light intensity, leaf temperature, air carbon dioxide concentration, and leaf diffusion resistance measured at five minute intervals. The steady-state calculations closely approximate the observed net photosynthesis rates for a broad range of weather conditions and leaf stomatal behavior.     

最优气孔行为理论和气孔导度模拟

气孔调节功能是陆地生态系统碳-水耦合过程中最重要的环节。与即时的气孔导度测量相比, 气孔导度斜率能有效地反映气孔导度对CO₂浓度、饱和水汽压亏缺和光合作用的敏感性, 包含了环境因子对光合作用和临界水分利用效率等的综合影响, 为研究全球变化下陆地生态系统碳-水耦合关系提供了一个简明且综合的框架。气孔导度模型从经验模型、半经验模型发展到机理模型, 经过很多学者的改进, 但是模型参数的生物学意义和变化规律还不明确。鉴于气孔导度斜率方面研究的重要性和研究的不足, 为了加强对气孔导度调节规律的认识, 并减少气孔导度模拟的不确定性, 该文主要综述了长期以来国内外关于最优气孔行为理论和气孔导度模拟方面的研究成果, 其中包括广泛使用的气孔导度模型及参数意义, 讨论影响气孔导度斜率的主要因素以及气孔导度机理模型的应用, 并对最优气孔行为理论和气孔导度模拟方面的研究做了简单展望。     

Ozone exposure causes a decoupling of conductance and photosynthesis: implications for the Ball-Berry stomatal conductance model

Industrialization has significantly altered atmospheric chemistry by increasing concentrations of chemicals such as nitrogen oxides (NO( x )) and volatile organic carbon, which react in the presence of sunlight to produce tropospheric ozone (O(3)). Ozone is a powerful oxidant that causes both visual and physiological damage to plants, impairing the ability of the plant to control processes like photosynthesis and transpiration. Damage to photosynthesis and stomatal conductance does not always occur at the same rate, which generates a problem when using the Ball-Berry model to predict stomatal conductance because the calculations directly rely on photosynthesis rates. The goals of this work were to develop a modeling framework to modify Ball-Berry stomatal conductance predictions independently of photosynthesis and to test the framework using experimental data. After exposure to elevated O(3) in open-top chambers, photosynthesis and stomatal conductance in tulip poplar changed at different rates through time. We were able to accurately model observed photosynthetic and stomatal conductance responses to chronic O(3) exposure in a Ball-Berry framework by adjusting stomatal conductance in addition to photosynthesis. This led to a significant improvement in the modeled ability to predict both photosynthesis and stomatal conductance responses to O(3).     

Optimal stomatal behavior theory for simulating stomatal conductance

Among the most critical processes in simulating terrestrial ecosystem performance is the regulatory role of stomata in carbon and water cycles. Compared with field measurements, the changes in stomatal slope caused by the biophysical environment provide a simple but effective synthetic framework for studying climate-related carbon and water cycling, due to its sensitivity to CO₂, vapor pressure deficit, and photosynthesis. It is also crucial in understanding the effects of climate change on photosynthesis and water use efficiency. Endeavored by numerous scholastic efforts, stomatal conductance models have been improved based on experimental, semi-experimental, and mechanical processes. However, the underlying biological mechanisms and the dynamics of key parameters in these models remain unexplored, especially regarding the changes in stomatal slope. By improving the understanding of the stomata’s regulatory role, we reduced the uncertainty of stomatal conductance simulation. We then synthesized the recent developments and lessons in optimal stomatal behavior theory to simulate stomatal conductance and included an introduction to widely used stomatal conductance models and parameters, the main factors influencing stomatal slopes, and applications of the mechanical stomatal conductance models in different ecosystems. Based on our literature review, we proposed that future research is needed on the optimal stomatal behavior theory and its applications in simulating stomatal conductance.     

Photosynthetic induction and leaf carbon gain in the tropical understorey epiphyte,Aspasia principissa

Gas exchange of the understorey epiphyte Aspasia principissa was studied in fluctuating light conditions both in the laboratory and in the field, testing the hypothesis that vascular epiphytes differ from most terrestrial understorey plants in showing a higher priority for water conservation. Consequently, a slow response of stomatal conductance to sudden increases in incident photon flux density (PFD) was expected, as was a fast loss of induction after such a light fleck. Results were only partly consistent with these expectations. Full induction of photosynthesis was indeed very slow and was not reached before, respectively, 40 and 60 min of saturating PFD in the field and the laboratory. In contrast, kinetics of induction loss were comparable with those of most terrestrial species studied to date. The overall impact of light flecks on in situ carbon gain again fulfilled expectations, being rather limited: the observed carbon gain was only approx. 66% of the potential carbon gain estimated from a square-wave response model. It is concluded that in the drought-prone epiphytic habitat of a moist lowland forest, water conservation takes priority over carbon gain, which severely limits the use of light flecks for CO(2) fixation in vascular epiphytes.     

The importance of mesophyll conductance in regulating forest ecosystem productivity during drought periods

Water availability is the most limiting factor to global plant productivity, yet photosynthetic responses to seasonal drought cycles are poorly understood, with conflicting reports on which limiting process is the most important during drought. We address the problem using a model‐data synthesis approach to look at canopy level fluxes, integrating twenty years of half hour data gathered by the FLUXNET network across six Mediterranean sites. The measured canopy level, water and carbon fluxes were used, together with an inverse canopy ecophysiological model, to estimate the bulk canopy conductance, bulk mesophyll conductance, and the canopy scale carbon pools in both the intercellular spaces and at the site of carboxylation in the chloroplasts. Thus the roles of stomatal and mesophyll conductance in the regulation of internal carbon pools and photosynthesis could be separated. A quantitative limitation analysis allowed for the relative seasonal responses of stomatal, mesophyll, and biochemical limitations to be gauged. The concentration of carbon in the chloroplast was shown to be a potentially more reliable estimator of assimilation rates than the intercellular carbon concentration. Both stomatal conductance limitations and mesophyll conductance limitations were observed to regulate the response of photosynthesis to water stress in each of the six species studied. The results suggest that mesophyll conductance could bridge the gap between conflicting reports on plant responses to soil water stress, and that the inclusion of mesophyll conductance in biosphere–atmosphere transfer models may improve their performance, in particular their ability to accurately capture the response of terrestrial vegetation productivity to drought.     

Leaf Gas Exchange in Canopy Species of a Venezuelan Cloud Forest

Tropical cloud forests are considered humid ecosystems with frequent cloud cover down to the ground surface. However, seasonal variation in precipitation may induce short-term water stress. For canopy leaves, this water stress may also be a consequence of large atmospheric vapor pressure deficits. The objective of this work was to study five canopy cloud forest species to determine if there are restrictions to leaf gas exchange as a consequence of seasonality in precipitation and to daily water deficit due to air evaporative demand mainly during maximum incoming radiation hours. Seasonal daily courses of microclimatic variables (air temperature, relative humidity, photosynthetic photon flux density) and plant responses (leaf water potential, stomatal conductance, CO₂ assimilation rates, leaf nitrogen concentration) were measured at 2400 m asl in Monterrey, an intermontane valley of the Venezuelan Andes. A gradient in terms of responses to water stress conditions was observed between the species, with Clusia multiflora (a 46% reduction in stomatal conductance between seasons) as the most affected and Miconia resimoides (increased stomatal conductance) responding more favorably to slight water stress conditions. If we consider the limitations of water stress and/or light conditions on CO₂ assimilation we may arrange the species into those in which water stress conditions have a greater impact on leaf carbon gain, those where light conditions are determinant and one in which both water stress and light conditions may affect leaf carbon assimilation.     

The diurnal time course of net photosynthesis of soybean leaves: Analysis with a physiologically based steady-state photosynthesis model

Summary A physiologically based steady-state model of whole leaf photosynthesis (WHOLEPHOT) is used to analyze observed net photosynthesis daily time courses of soybean, Glycine max (L.) Merr., leaves. Observations during two time periods of the 1978 growing season are analyzed and compared. After adjustment of the model for soybean, net photosynthesis rates are calculated with the model in response to measured incident light intensity, leaf temperature, air carbon dioxide concentration, and leaf diffusion resistance. The steady-state calculations closely approximate observed net photosynthesis. Results of the comparison reveal a decrease in photosynthetic capacity in leaves sampled during the second time period, which is associated with decreasing ability of leaves to respond to light intensity and internal air space carbon dioxide concentration, increasing mesophyll resistance, and increasing stomatal resistance.     

半干旱地区3种植物叶片水平的抗旱耐旱特性分析——两个气孔导度模型的应用和比较

在对半干旱区3种植物进行生理生态特性测定的基础上,应用两种气孔导度模型进行参数的非线性拟合,BBL模型平均可以解释77.6%的结果,Gao模型平均可以解释59.3%的结果。但Gao模型作为一个机理性的模型,其参数具有明确的物理意义。模型的行为和敏感性分析结果说明,用BBL计算的气孔导度一般大于Gao模型。BBL模型对于干旱胁迫下的土壤水分亏缺没有响应, 因而不适合用作干旱半干旱区的植物生理生态学分析和生态系统模拟。而Gao模型可以描述在各种水分条件下植物气孔导度的响应。Gao模型的结果说明,与油松 (Pinus tabulaeformis) 和中间锦鸡儿 (Caragana intermedia) 比较,小叶杨 (Populus simonii) 具有最小的抗旱和耐旱能力,油松具有最好的叶片水平的耐旱和抗旱特性,但其气孔导度对土壤水分的不敏感意味着在干旱条件下维持光合作用的同时,也可能会导致过多的水分损失。中间锦鸡儿具有很强的耐旱性,且其气孔导度对土壤水分的变化敏感,二者相结合,中间锦鸡儿可以在土壤水分条件较好的情况下,维持较大的气孔导度以满足光合作用的需要,但在土壤水分胁迫严重的时候能迅速降低气孔导度以保持土壤水分。     

黄土高原森林草原区6种植物光合特性研究

 对黄土高原森林草原区6种不同植物的生理生态学特性进行了一个生长季的野外观测。测定了2002年生长季早、中、晚期植物叶片的光合、蒸腾速率及相应的微气象因子和土壤水分的含量。在此基础上,采用机理性生理生态学模型对黄土高原森林草原区6种植物净光合速率和气孔导度与环境因子的关系进行了分析,净光合速率模型和气孔导度模型分别能够解释57%～79% 和40%～59% 生长季中净光合速率和气孔导度的日变化。在此基础上根据拟合得到的参数计算了典型7月份天气的净光合速率的日变化。模拟的结果表明：沙棘(Hippophae rhamnoides L. subsp. sinensis Rousi)的生物化学光合能力最强,茵陈蒿（Artemisia capillaris）的光呼吸速率最低,这两种植物的净光合速率高于其它植物种。刺槐（Robinia pseudoacacia）、铁杆蒿 (Artemisia gmelinii)、茵陈蒿和沙棘在午后出现的净光合速率下降主要是由气孔导度减小引起的,而苹果 (Malus pumila) 和柠条 (Caragana korshinskii)午后净光合速率的降低与叶肉细胞酶的活性降低有关。这些结论为未来的实验室测定提供了野外观测佐证。     

额济纳荒漠河岸胡杨林叶片气孔导度与微环境因子关系的模拟研究

以额济纳荒漠河岸胡杨(Populus euphratica)为研究对象,利用LI-6400光合测定仪于2005年5~9月份观测了胡杨叶片气体交换数据,研究了胡杨叶片气孔导度与光合速率、光合有效辐射与光合速率之间的关系.结果表明:(1)胡杨叶片净光合速率随气孔导度的增大而升高,但当气孔导度增加到一定值后,光合速率的增加变缓慢直至平稳,并主要是非气孔限制因素造成的;Ball-Berry模型(B-B模型)能够很好地描述气孔导度与光合速率之间的关系(R2=0.92).(2)叶片净光合速率随着有效辐射的变化符合非直角双曲线规律(R2=0.99).(3)B-B模型和非直角双曲线光合模型耦合后模拟值与观测值之间存在很好的正相关性(r=0.93),但耦合模型的模拟值还是较实测值偏大.因此,在干旱区还必须考虑水分限制因素对气孔开闭的控制作用,进一步构建适合干旱区生态系统特点的水-碳耦合循环机理模型.     

Simulation of leaf photosynthesis of C3 plants under fluctuating light and different temperatures

An induction-dependent empirical model was developed to simulate the C₃ leaf photosynthesis under fluctuating light and different temperatures. The model also takes into account the stomatal conductance when the light intensity just exceeds the compensation point after a prolonged period of darkness (initial stomatal conductance, $ g_{{{\text{S}}_{\text{ini}} }} $ ). The model was parameterized for both Chrysanthemum morifolium and Spinacia oleracea by artificially changing the induction states of the leaves in the climate chamber. The model was tested under natural conditions that were including frequent light flecks due to partial cloud cover and varying temperatures. The temporal course of observed photosynthesis rate and the carbon gain was compared to the simulation. The ability of the current model to predict the carbon assimilation rate was assessed using different statistical indexes. The model predictions were accurate but the model slightly underestimated the actual overall carbon gain. The accuracy of the simulation was largely dependent on the parameters that were calculated for the particular plant species, of which the simulation is intended for. In particular, the rate of change of induction and the initial stomatal conductance were found to be highly important and these were species-specific parameters for the predictions. The model is suitable for estimating instantaneous leaf CO₂ assimilation for different herbaceous plant species under dynamic environmental conditions. It can be simply calibrated for other crops, by estimating the individual parameters.