Phylogenetic signal and climatic niche of stem photosynthesis in the mediterranean and desert regions of California and Baja California Peninsula.

PREMISE: Woody plants with photosynthetic stems are common in the drylands of the world; however, we know little about the origin(s) and geographical distribution of photosynthetic stems. Therefore, we set to answer the following questions: (1) Is stem photosynthesis phylogenetically conserved? (2) Do green-stemmed and fleshy-stemmed species have identifiable climatic niches? METHODS: We mapped the photosynthetic stem trait onto a phylogeny of 228 mediterranean and desert species and calculated indices of phylogenetic signal and created climatic niche models of 28 species belonging to three groups: green, fleshy, and green-and-fleshy stemmed species. RESULTS: We found phylogenetic signal in the fleshy stem trait, but not in the green stem trait. Fleshy-stemmed species occupy areas associated with high isothermality, high precipitation seasonality, and high mean temperature of the wettest quarter, whereas green-stemmed species occupy areas associated with high precipitation of driest month, high precipitation of coldest quarter, high mean diurnal temperature range and high maximum temperature of the warmest month. CONCLUSIONS: Despite the fact that both photosynthetic stem types help cope with water shortage, having fleshy stems allows plants to cope with greater precipitation seasonality than is possible with green stems. Green stems require a lot of water to be stored in the soil to maintain net photosynthesis during the dry season, so they inhabit areas with higher and more predictable precipitation.

Woody tissue photosynthesis delays drought stress in Populus tremula trees and maintains starch reserves in branch xylem tissues.

Photosynthesis in woody tissues (Pwt ) is less sensitive to water shortage than in leaves, hence, Pwt might be a crucial carbon source to alleviate drought stress. To evaluate the impact of Pwt on tree drought tolerance, woody tissues of 4-m-tall drought-stressed Populus tremula trees were subjected to a light-exclusion treatment across the entire plant to inhibit Pwt . Xylem water potential (Ψxylem ), sap flow ( FH2O ), leaf net photosynthesis (Pn,l ), stem diameter variations (ΔD), in vivo acoustic emissions in stems (AEs) and nonstructural carbohydrate concentrations ([NSC]) were monitored to comprehensively assess water and carbon relations at whole-tree level. Under well-watered conditions, Pwt kept Ψxylem at a higher level, lowered FH2O and had no effect on [NSC]. Under drought, Ψxylem , FH2O and Pn,l in light-excluded trees rapidly decreased in concert with reductions in branch xylem starch concentration. Moreover, sub-daily patterns of ΔD, FH2O and AEs were strongly related, suggesting that in vivo AEs may inform not only about embolism events, but also about capacitive release and replenishment of stem water pools. Results highlight the importance of Pwt in maintaining xylem hydraulic integrity under drought conditions and in sustaining NSC pools to potentially limit increases in xylem tension.

Corticular photosynthesis drives bark water uptake to refill embolized vessels in dehydrated branches of Salix matsudana.

It is well known that xylem embolism can be repaired by bark water uptake and that the sugar required for embolism refilling can be provided by corticular photosynthesis. However, the relationship between corticular photosynthesis and embolism repair by bark water uptake is still poorly understood. In this study, the role of corticular photosynthesis in embolism repair was assessed using Salix matsudana branch segments dehydrated to -1.9 MPa (P50 , water potential at 50% loss of conductivity). The results indicated that corticular photosynthesis significantly promoted water uptake and nonstructural carbohydrate (NSC) accumulation in the bark and xylem during soaking, thereby effectively enhancing the refilling of the embolized vessels and the recovery of hydraulic conductivity. Furthermore, the influence of the extent of dehydration on the embolism refilling enhanced by corticular photosynthesis was investigated. The enhanced refilling effects were much higher in the mildly dehydrated (-1.5 MPa) and moderately dehydrated (-1.9 MPa) branch segments than in the severely dehydrated (-2.2 MPa) branch segments. This study provides evidence that corticular photosynthesis plays a crucial role in xylem embolism repair by bark water uptake for mildly and moderately dehydrated branches.

More than just CO2 -recycling: corticular photosynthesis as a mechanism to reduce the risk of an energy crisis induced by low oxygen.

Reassimilation of internal CO2 via corticular photosynthesis (PScort ) has an important effect on the carbon economy of trees. However, little is known about its role as a source of O2 supply to the stem parenchyma and its implications in consumption and movement of O2 within trees. PScort of young Populus nigra (black poplar) trees was investigated by combining optical micro-optode measurements with monitoring of stem chlorophyll fluorescence. During times of zero sap flow in spring, stem oxygen concentrations (cO2 ) exhibited large temporal changes. In the sapwood, over 80% of diurnal changes in cO2 could be explained by respiration rates (Rd(mod) ). In the cortex, photosynthetic oxygen release during the day altered this relationship. With daytime illumination, oxygen levels in the cortex steadily increased from subambient and even exhibited a diel period of superoxia of up to 110% (% air sat.). By contrast, in the sapwood, cO2 never reached ambient levels; the diurnal oxygen deficit was up to 25% of air saturation. Our results confirm that PScort is not only a CO2 -recycling mechanism, it is also a mechanism to actively raise the cortical O2 concentration and counteract temporal/spatial hypoxia inside plant stems.

Proteomic insights into the photosynthetic divergence between bark and leaf chloroplasts in Salix matsudana.

Bark chloroplasts play important roles in carbon balancing by recycling internal stem CO2 into assimilated carbon. The photosynthetic response of bark chloroplasts to interior stem environments has been studied recently in woody plants. However, the molecular regulatory mechanisms underlying specific characteristics of bark photosynthesis remain unclear. To address this knowledge gap, differences in the structure, photosynthetic activity and protein expression profiles between bark and leaf chloroplasts were investigated in Salix matsudana in this study. Bark chloroplasts exhibited broader and lower grana stacks and higher levels of starch relative to leaf chloroplasts. Concomitantly, decreased oxygen evolution rates and decreased saturated radiation point were observed in bark chloroplasts. Furthermore, a total of 293 differentially expressed proteins (DEPs) were identified in bark and leaf chloroplast profile comparisons. These DEPs were significantly enriched in photosynthesis-related biological processes or Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways associated with photosynthesis. All 116 DEPs within the KEGG pathways associated with photosynthesis light reactions were downregulated in bark chloroplasts, including key proteins responsible for chlorophyll synthesis, light energy harvesting, nonphotochemical quenching, linear electron transport and photophosphorylation. Interestingly, seven upregulated proteins involved in dark reactions were identified in bark chloroplasts that comprised two kinds of malic enzymes typical of C4-type photosynthesis. These results provide comprehensive proteomic evidence to understand the low photochemical capability of bark chloroplasts and suggest that bark chloroplasts might fix CO2 derived from malate decarboxylation.

Functional characterization of the corticular photosynthetic apparatus in grapevine.

A comparative analysis of functional characteristics of the grapevine leaf photosynthetic apparatus (LPA) and corticular photosynthetic apparatus (CPA) in chlorenchyma tissues of first-year lignified vine was performed. Obtained results demonstrate significant differences between the functional properties of the CPA and the LPA. CPA contains an increased proportion (about 2/3) of QB-non-reducing centers of photosystem II (PSII) that is confirmed by elevated O-J phase in fluorescence kinetics, high PSIIß content, and slower QA-• reoxidation. CPA and LPA use different strategies to utilize absorbed light energy and to protect itself against excessive light. CPA dissipates a significant proportion of absorbed light energy as heat (regulated and non-regulated dissipation), and only a smaller part of the excitation energy is used in the dark stages of photosynthesis. The rate constant of photoinhibition and fluorescence quenching due to photoinhibition in CPA is almost three times higher than in LPA, while high-energy state fluorescence quenching value is twice lower. The saturation of vine chlorenchyma tissue with water increases the CPA tolerance to photoinhibition and promotes the ability to restore the photosynthetic activity after photoinhibition. The electron microscopy analysis confirmed the presence of intact plastids in vine chlorenchyma tissue, the interior space of plastids is filled with large starch grains while bands of stacked thylakoid membranes are mainly localized on the periphery. Analyzes showed that corticular plastids are specialized organelles combining features of chloroplasts, amyloplasts and gerontoplasts. Distinct structural organization of photosynthetic membranes and microenvironment predetermine distinctive functional properties of CPA.

Chloroplast Distribution in the Stems of 23 Eucalypt Species.

Small diameter branchlets and smooth barked stems and branches of most woody plants have chloroplasts. While the stems of several eucalypt species have been shown to photosynthesise, the distribution of chloroplasts has not been investigated in detail. The distribution of chloroplasts in branchlets (23 species) and larger diameter stems and branches with smooth bark (14 species) was investigated in a wide range of eucalypts (species of Angophora, Corymbia and Eucalyptus) using fresh hand sections and a combination of bright field and fluorescence microscopy. All species had abundant stem chloroplasts. In both small and large diameter stems, the greatest concentration of chloroplasts was in a narrow band (usually 100-300 µm thick) immediately beneath the epidermis or phellem. Deeper chloroplasts were present but at a lower density due to abundant fibres and sclereids. In general, chloroplasts were found at greater depths in small diameter stems, often being present in the secondary xylem rays and the pith. The cells of the chlorenchyma band were small, rounded and densely packed, and unlike leaf mesophyll. A high density of chloroplasts was found just beneath the phellem of large diameter stems. These trees gave no external indication that green tissues were present just below the phellem. In these species, a thick phellem was not present to protect the inner living bark. Along with the chlorenchyma, the outer bark also had a high density of fibres and sclereids. These sclerenchyma cells probably disrupted a greater abundance and a more organised arrangement of the cells containing chloroplasts. This shows a possible trade-off between photosynthesis and the typical bark functions of protection and mechanical strength.

Tree Species with Photosynthetic Stems Have Greater Nighttime Sap Flux.

An increasing body of evidence has shown that nighttime sap flux occurs in most plants, but the physiological implications and regulatory mechanism are poorly known. The significance of corticular photosynthesis has received much attention during the last decade, however, the knowledge of the relationship between corticular photosynthesis and nocturnal stem sap flow is limited at present. In this study, we divided seven tree species into two groups according to different photosynthetic capabilities: trees of species with (Castanopsis hystrix, Michelia macclurei, Eucalyptus citriodora, and Eucalyptus grandis × urophylla) and without (Castanopsis fissa, Schima superba, and Acacia auriculiformis) photosynthetic stems, and the sap flux (Js) and chlorophyll fluorescence parameters for these species were measured. One-way ANOVA analysis showed that the Fv/Fm (Maximum photochemical quantum yield of PSII) and ΦPSII (effective photochemical quantum yield of PSII) values were lower in non-photosynthetic stem species compared to photosynthetic stem species. The linear regression analysis showed that Js,d (daytime sap flux) and Js,n (nighttime sap flux) of non-photosynthetic stem species was 87.7 and 60.9% of the stem photosynthetic species. Furthermore, for a given daytime transpiration water loss, total nighttime sap flux was higher in species with photosynthetic stems (SlopeSMA = 2.680) than in non-photosynthetic stems species (SlopeSMA = 1.943). These results mean that stem corticular photosynthesis has a possible effect on the nighttime water flow, highlighting the important eco-physiological relationship between nighttime sap flux and corticular photosynthesis.

Carbon isotope discrimination in photosynthetic bark.

We developed and tested a theoretical model describing carbon isotope discrimination during photosynthesis in tree bark. Bark photosynthesis reduces losses of respired CO2 from the underlying stem. As a consequence, the isotopic composition of source CO2 and the CO2 concentration around the chloroplasts are quite different from those of photosynthesizing leaves. We found three lines of evidence that bark photosynthesis discriminates against 13C. First, in bark of Populus tremuloides, the δ13C of CO2 efflux increased from -24.2‰ in darkness to -15.8‰ in the light. In Pinus monticola, the δ13C of CO2 efflux increased from -27.7‰ in darkness to -10.2‰ in the light. Observed increases in δ13C were generally in good agreement with predictions from the theoretical model. Second, we found that δ13C of dark-respired CO2 decreased following 2-3 h of illumination (P<0.01 for Populus tremuloides, P<0.001 for Pinus monticola). These decreases suggest that refixed photosynthate rapidly mixes into the respiratory substrate pool. Third, a field experiment demonstrated that bark photosynthesis influenced whole-tissue δ13C. Long-term light exclusion caused a localized increase in the δ13C of whole bark and current-year wood in branches of P. monticola (P<0.001 and P<0.0001, respectively). Thus bark photosynthesis was shown to discriminate against 13C and create a pool of photosynthate isotopically lighter than the dark respiratory pool in all three experiments. Failure to account for discrimination during bark photosynthesis could interfere with interpretation of the δ13C in woody tissues or in woody-tissue respiration.