skip to main content

Title: Light Potentials of Photosynthetic Energy Storage in the Field: What limits the ability to use or dissipate rapidly increased light energy?
The responses of plant photosynthesis to rapid fluctuations in environmental conditions are thought to be critical for efficient conversion of light energy. Such responses are not well represented under laboratory conditions, but have also been difficult to probe in complex field environments. We demonstrate an open science approach to this problem that combines multifaceted measurements of photosynthesis and environmental conditions, and an unsupervised statistical clustering approach. In a selected set of data on mint (Mentha sp.), we show that the “light potential” for increasing linear electron flow (LEF) and nonphotochemical quenching (NPQ) upon rapid light increases are strongly suppressed in leaves previously exposed to low ambient PAR or low leaf temperatures, factors that can act both independently and cooperatively. Further analyses allowed us to test specific mechanisms. With decreasing leaf temperature or PAR, limitations to photosynthesis during high light fluctuations shifted from rapidly-induced NPQ to photosynthetic control (PCON) of electron flow at the cytochrome b6f complex. At low temperatures, high light induced lumen acidification, but did not induce NPQ, leading to accumulation of reduced electron transfer intermediates, a situation likely to induce photodamage, and represents a potential target for improving the efficiency and robustness of photosynthesis. Finally, we discuss the implications of the approach for open science efforts to understand and improve crop productivity.  more » « less
Award ID(s):
Author(s) / Creator(s):
; ; ; ; ;
Date Published:
Journal Name:
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Drought is among the most damaging climate extremes, potentially causing significant decline in ecosystem functioning and services at the regional to global scale, thus monitoring of drought events is critically important. Solar‐induced chlorophyll fluorescence (SIF) has been found to strongly correlate with gross primary production on the global scale. Recent advances in the remote sensing of SIF allow for large‐scale, real‐time estimation of photosynthesis using this relationship. However, several studies have used SIF to quantify the impact of drought with mixed results, and the leaf‐level mechanisms linking SIF and photosynthesis are unclear, particularly how the relationship may change under drought. We conducted a drought experiment with 2‐yr oldPopulus deltoides. We measured leaf‐level gas exchange, SIF, and pulse amplitude modulated (PAM) fluorescence before and during the 1‐month drought. We found clear responses of net photosynthesis and stomatal conductance to water stress, however, SIF showed a smaller response to drought. Net photosynthesis (Anet) and conductance dropped 94% and 95% on average over the drought, while SIF values only decreased slightly (21%). Electron transport rate dropped 64% when compared to the control over the last week of drought, but the electron transport chain did not completely shut down asAnetapproached zero. Additionally, SIF yield (SIFy) was positively correlated with steady‐state fluorescence (Fs) and negatively correlated with non‐photochemical quenching (NPQ;R2 = 0.77). BothFsand SIFy, after normalization by the minimum fluorescence from a dark‐adapted sample (Fo), showed a more pronounced drought response, although the results suggest the response is complicated by several factors. Leaf‐level experiments can elucidate mechanisms behind large‐scale remote sensing observations of ecosystem functioning. The value of SIF as an accurate estimator of photosynthesis may decrease during mild stress events of short duration, especially when the response is primarily stomatal and not fully coupled with the light reactions of photosynthesis. We discuss potential factors affecting the weak SIF response to drought, including upregulation of NPQ, change in internal leaf structure and chlorophyll concentration, and photorespiration. The results suggest that SIF is mainly controlled by the light reactions of photosynthesis, which operate on different timescales than the stomatal response.

    more » « less
  2. The capacity of photoautotrophs to fix carbon depends on the efficiency of the conversion of light energy into chemical potential by photosynthesis. In nature, light input into photosynthesis can change very rapidly and dramatically. To analyze how genetic variation in Arabidopsis thaliana affects photosynthesis and growth under dynamic light conditions, 36 randomly chosen natural accessions were grown under uniform and fluctuating light intensities. After 14 days of growth under uniform or fluctuating light regimes, maximum photosystem II quantum efficiency (Fv/Fm) was determined, photosystem II operating efficiency (ΦPSII) and non-photochemical quenching (NPQ) were measured in low light, and projected leaf area (PLA) as well as the number of visible leaves were estimated. Our data show that ΦPSII and PLA were decreased and NPQ was increased, while Fv/Fm and number of visible leaves were unaffected, in most accessions grown under fluctuating compared to uniform light. There were large changes between accessions for most of these parameters, which, however, were not correlated with genomic variation. Fast growing accessions under uniform light showed the largest growth reductions under fluctuating light, which correlated strongly with a reduction in ΦPSII, suggesting that, under fluctuating light, photosynthesis controls growth and not vice versa. 
    more » « less
  3. Abstract

    Sigma factor (SIG) proteins contribute to promoter specificity of the plastid‐encodedRNApolymerase during chloroplast genome transcription. All six members of theSIGfamily, that is,SIG1–SIG6, are nuclear‐encoded proteins targeted to chloroplasts. Sigma factor 2 (SIG2) is a phytochrome‐regulated protein important for stoichiometric control of the expression of plastid‐ and nuclear‐encoded genes that impact plastid development and plant growth and development. AmongSIGfactors,SIG2 is required not only for transcription of chloroplast genes (i.e., anterograde signaling), but also impacts nuclear‐encoded, photosynthesis‐related, and light signaling‐related genes (i.e., retrograde signaling) in response to plastid functional status. AlthoughSIG2 is involved in photomorphogenesis in Arabidopsis, the molecular bases for its role in light signaling that impacts photomorphogenesis and aspects of photosynthesis have only recently begun to be investigated. Previously, we reported thatSIG2 is necessary for phytochrome‐mediated photomorphogenesis specifically under red (R) and far‐red light, thereby suggesting a link between phytochromes and nuclear‐encodedSIG2 in light signaling. To explore transcriptional roles ofSIG2 in R‐dependent growth and development, we performedRNAsequencing analysis to compare gene expression insig2‐2mutant and Col‐0 wild‐type seedlings at two developmental stages (1‐ and 7‐day). We identified a subset of misregulated genes involved in growth, hormonal cross talk, stress responses, and photosynthesis. To investigate the functional relevance of these gene expression analyses, we performed several comparative phenotyping tests. In these analyses, strongsig2mutants showed insensitivity to bioactiveGA3, high intracellular levels of hydrogen peroxide (H2O2) indicative of a stress response, and specific defects in photosynthesis, including elevated levels of cyclic electron flow (CEF) and nonphotochemical quenching (NPQ). We demonstrated thatSIG2 regulates a broader range of physiological responses at the molecular level than previously reported, with specific roles in red‐light‐mediated photomorphogenesis.

    more » « less
  4. Abstract

    In nature, plants experience rapid changes in light intensity and quality throughout the day. To maximize growth, they have established molecular mechanisms to optimize photosynthetic output while protecting components of the light‐dependent reaction and CO2fixation pathways. Plant phenotyping of mutant collections has become a powerful tool to unveil the genetic loci involved in environmental acclimation. Here, we describe the phenotyping of the transfer‐DNA (T‐DNA) insertion mutant line SALK_008491, previously known asnhd1‐1. Growth in a fluctuating light regime caused a loss in growth rate accompanied by a spike in photosystem (PS) II damage and increased non‐photochemical quenching (NPQ). Interestingly, an independentnhd1null allele did not recapitulate the NPQ phenotype. Through bulk sequencing of a backcrossed segregating F2pool, we identified an ~14‐kb large deletion on chromosome 3 (Chr3) in SALK_008491 affecting five genes upstream ofNHD1. BesidesNHD1, which encodes for a putative plastid Na+/H+antiporter, the stromal NAD‐dependent D‐3‐phosphoglycerate dehydrogenase 3 (PGDH3) locus was eradicated. Although some changes in the SALK_008491 mutant's photosynthesis can be assigned to the loss of PGDH3, our follow‐up studies employing respective single mutants and complementation with overlapping transformation‐competent artificial chromosome (TAC) vectors reveal that the exacerbated fluctuating light sensitivity in SALK_008491 mutants result from the simultaneous loss of PGDH3 and NHD1. Altogether, the data obtained from this large deletion‐carrying mutant provide new and unintuitive insights into the molecular mechanisms that function to protect the photosynthetic machinery. Moreover, our study renews calls for caution when setting up reverse genetic studies using T‐DNA lines. Although second‐site insertions, indels, and SNPs have been reported before, large deletion surrounding the insertion site causes yet another problem. Nevertheless, as shown through this research, such unpredictable genetic events following T‐DNA mutagenesis can provide unintuitive insights that allow for understanding complex phenomena such as the plant acclimation to dynamic high light stress.

    more » « less
  5. Organismal phenotypes often co-vary with environmental variables across broad geographic ranges. Less is known about the extent to which phenotypes match local conditions when multiple biotic and abiotic stressors vary at fine spatial scales. Bittercress (Brassicaceae: Cardamine cordifolia), a perennial forb, grows across a microgeographic mosaic of two contrasting herbivory regimes: high herbivory in meadows (sun habitats) and low herbivory in deeply shaded forest understories (shade habitats). We tested for local phenotypic differentiation in plant size, leaf morphology, and anti-herbivore defense (realized resistance and defensive chemicals, i.e., glucosinolates) across this habitat mosaic through reciprocal transplant–common garden experiments with clonally propagated rhizomes. We found habitat-specific divergence in morphological and defensive phenotypes that manifested as contrasting responses to growth in shade common gardens: weak petiole elongation and attenuated defenses in populations from shade habitats, and strong petiole elongation and elevated defenses in populations from sun habitats. These divergent phenotypes are generally consistent with reciprocal local adaptation: plants from shade habitats that naturally experience low herbivory show reduced investment in defense and an attenuated shade avoidance response, owing to its ineffectiveness within forest understories. By contrast, plants from sun habitats with high herbivory show shade-induced elongation, but no evidence of attenuated defenses canonically associated with elongation in shade-intolerant plant species. Finally, we observed differences in flowering phenology between habitat types that could potentially contribute to inter-habitat divergence by reducing gene flow. This study illuminates how clonally heritable plant phenotypes track a fine-grained mosaic of herbivore pressure and light availability in a native plant. 
    more » « less