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Leaves are the major plant tissue for transpiration and carbon fixation in deciduous trees. In harsh habitats, atmospheric CO2 assimilation via stem photosynthesis is common, providing extra carbon gain to cope with the detrimental conditions. We studied two almond species, the commercial Prunus dulcis cultivar "Um-el-Fahem" and the rare wild Prunus arabica. Our study revealed two distinctive strategies for carbon gain in these almond species. While, in P. dulcis, leaves possess the major photosynthetic surface area, in P. arabica, green stems perform this function, in particular during the winter after leaf drop. These two species' anatomical and physiological comparisons show that P. arabica carries unique features that support stem gas exchange and high-gross photosynthetic rates via stem photosynthetic capabilities (SPC). On the other hand, P. dulcis stems contribute low gross photosynthesis levels, as they are designed solely for reassimilation of CO2 from respiration, which is termed stem recycling photosynthesis (SRP). Results show that (a) P. arabica stems are covered with a high density of sunken stomata, in contrast to the stomata on P. dulcis stems, which disappear under a thick peridermal (bark) layer by their second year of development. (b) P. arabica stems contain significantly higher levels of chlorophyll compartmentalized to a mesophyll-like, chloroplast-rich, parenchyma layer, in contrast to rounded-shape cells of P. dulcis's stem parenchyma. (c) Pulse amplitude-modulated (PAM) fluorometry of P. arabica and P. dulcis stems revealed differences in the chlorophyll fluorescence and quenching parameters between the two species. (d) Gas exchange analysis showed that guard cells of P. arabica stems tightly regulate water loss under elevated temperatures while maintaining constant and high assimilation rates throughout the stem. Our data show that P. arabica uses a distinctive strategy for tree carbon gain via stem photosynthetic capability, which is regulated efficiently under harsh environmental conditions, such as elevated temperatures. These findings are highly important and can be used to develop new almond cultivars with agriculturally essential traits.

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Water availability could alter multiple ecophysiological processes such as water use strategy, photosynthesis, and respiration, thereby modifying plant water use and carbon gain. However, a lack of field observations hinders our understanding of how water availability affects stem photosynthesis at both organ and plant levels of desert shrubs. In this study, we measured gas exchange and oxygen stable isotopes to quantify water sources, stem recycling photosynthesis, and whole-plant carbon balance in two coexisting Haloxylon species (Haloxylon ammodendron and Haloxylon persicum) at different groundwater depths in the Gurbantonggut Desert. The overall aim of the study was to analyze and quantify the important role of stem recycling photosynthesis for desert shrubs (Haloxylon species) under different groundwater depths. The results showed that (1) regardless of changes in groundwater depth, H. ammodendron consistently used groundwater and H. persicum used deep soil water as their main water source, with greater than 75% of xylem water being derived from groundwater and deep soil water for the two species, respectively; (2) stem recycling photosynthesis refixed 72-81% of the stem dark respiration, and its contribution to whole-plant carbon assimilation was 10-21% for the two species; and (3) deepened groundwater increased stem water use efficiency and its contribution to whole-plant carbon assimilation in H. persicum but not in H. ammodendron. Our study provided observational evidence that deepened groundwater depth induced H. persicum to increase stem recycling photosynthetic capacity and a greater contribution to whole-plant carbon assimilation, but this did not occur on H. ammodendron. Our study indicates that stem recycling photosynthesis may play an important role in the survival of desert shrubs in drought conditions.

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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.

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Woody tissue photosynthesis (Pwt) contributes to the tree carbon (C) budget and generally stimulates radial stem growth under ambient atmospheric CO2 concentration (aCO2). Moreover, Pwt has potential to enhance tree survival under changing climates by delaying negative effects of drought stress on tree hydraulic functioning. However, the relevance of Pwt on tree performance under elevated atmospheric CO2 concentration (eCO2) remains unexplored. To fill this knowledge gap, 1-year-old Populus tremula L. seedlings were grown in two treatment chambers at aCO2 and eCO2 (400 and 660 ppm, respectively), and woody tissues of half of the seedlings in each treatment chamber were light-excluded to prevent Pwt. Radial stem growth, sap flow, leaf photosynthesis and stomatal and canopy conductance were measured throughout the growing season, and the concentration of non-structural carbohydrates (NSC) in stem tissues was determined at the end of the experiment. Fuelled by eCO2, an increase in stem growth of 18 and 50% was observed in control and light-excluded trees, respectively. Woody tissue photosynthesis increased radial stem growth by 39% under aCO2, while, surprisingly, no impact of Pwt on stem growth was observed under eCO2. By the end of the growing season, eCO2 and Pwt had little effect on stem growth, leaf photosynthesis acclimated to eCO2, but stomatal conductance did not, and homeostatic stem NSC pools were observed among combined treatments. Our results highlight that eCO2 potentially fulfils plant C requirements, limiting the contribution of Pwt to stem growth as atmospheric [CO2] rises, and that radial stem growth in young developing trees was C (source) limited during early phenological stages but transitioned towards sink-driven control at the end of the growing season.

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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.

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A substantial portion of locally respired CO2 in stems can be assimilated by chloroplast-containing tissues. Woody tissue photosynthesis (Pwt ) therefore plays a major role in the stem carbon balance. To study the impact of Pwt on stem carbon cycling along a gradient of water availability, stem CO2 efflux (EA ), xylem CO2 concentration ([CO2 ]), and xylem water potential (Ψxylem ) were measured in 4-year-old Populus tremula L. trees exposed to drought stress and different regimes of light exclusion of woody tissues. Under well-watered conditions, local Pwt decreased EA up to 30%. Axial CO2 diffusion (Dax ) induced by distant Pwt caused an additional decrease in EA of up to 25% and limited xylem [CO2 ] build-up. Under drought stress, absolute decreases in EA driven by Pwt remained stable, denoting that Pwt was not affected by drought. At the end of the dry period, when transpiration was low, local Pwt and Dax offset 20% and 10% of stem respiration on a daily basis, respectively. These results highlight (a) the importance of Pwt for an adequate interpretation of EA measurements and (b) homeostatic Pwt along a drought stress gradient, which might play a crucial role to fuel stem metabolism when leaf carbon uptake and phloem transport are limited.

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