Since the first description of phloem sap composition nearly 60 years ago, it is generally assumed that phloem sap does not contain nitrate and that there is little or no backflow of nitrate from shoots to roots. While it is true that nitrate can occasionally be absent from phloem sap, there is now substantial evidence that phloem can carry nitrate and furthermore, transporters involved in nitrate redistribution to shoot sink organs and roots have been found. This raises the question of why nitrate may or may not be present in phloem sap, why its concentration is generally kept low, and whether plant shoot-root nutrient cycling also involves nitrate. We propose here that phloem sap nitrate is not only an essential component of plant nutritional signaling but also contributes to physical properties of phloem sap and as such, its concentration is controlled to ensure proper coordination of plant development and nutrient transport.
Atmospheric and climate change will expose tropical forests to conditions they have not experienced in millions of years. To better understand the consequences of this change we studied photosynthetic acclimation of the neotropical tree species Tabebuia rosea to combined 4°C warming and twice-ambient (800 ppm) CO2. We measured temperature responses of the maximum rates of ribulose 1,5-bisphosphate carboxylation (VCMax), photosynthetic electron transport (JMax), net photosynthesis (PNet), and stomatal conductance (gs), and fitted the data using a probabilistic Bayesian approach. To evaluate short-term acclimation plants were then switched between treatment and control conditions and re-measured after 1–2 weeks. Consistent with acclimation, the optimum temperatures (TOpt) for VCMax, JMax and PNet were 1–5°C higher in treatment than in control plants, while photosynthetic capacity (VCMax, JMax, and PNet at TOpt) was 8–25% lower. Likewise, moving control plants to treatment conditions moderately increased temperature optima and decreased photosynthetic capacity. Stomatal density and sensitivity to leaf-to-air vapor pressure deficit were not affected by growth conditions, and treatment plants did not exhibit stronger stomatal limitations. Collectively, these results illustrate the strong photosynthetic plasticity of this tropical tree species as even fully-developed leaves of saplings transferred to extreme conditions partially acclimated.
Opportunistic diversification has allowed ferns to radiate into epiphytic niches in angiosperm dominated landscapes. However, our understanding of how ecophysiological function allowed establishment in the canopy and the potential transitionary role of the hemi-epiphytic life form remain unclear. Here, we surveyed 39 fern species in Costa Rican tropical forests to explore epiphytic trait divergence in a phylogenetic context. We examined leaf responses to water deficits in terrestrial, hemi-epiphytic, and epiphytic ferns and related these findings to functional traits that regulate leaf water status. Epiphytic ferns had reduced xylem area (-63%), shorter stipe lengths (-56%), thicker laminae (+41%), and reduced stomatal density (-46%) compared to terrestrial ferns. Epiphytic ferns exhibited similar turgor loss points, higher osmotic potential at saturation, and lower tissue capacitance after turgor loss than terrestrial ferns. Overall, hemi-epiphytic ferns exhibited traits that share characteristics of both terrestrial and epiphytic species. Our findings clearly demonstrate the prevalence of water conservatism in both epiphytic and hemi-epiphytic ferns, via selection for anatomical and structural traits that avoid leaf water stress. Even with likely canalized physiological function, adaptations for drought avoidance have allowed epiphytic ferns to successfully endure the stresses of the canopy habitat.
Effects of K deficiency have been investigated for several decades and recently, progress has been made in identifying metabolomics signatures thereby offering potential to monitor the K status of crops in the field. However, effects of low K conditions could also be due to the antagonism with other nutrients like calcium (Ca) and the well-known biomarker of K deficiency, putrescine, could be a response to Ca/K imbalance rather than K deficiency. We carried out experiments in sunflower grown at either low or high K, at high or low Ca, with or without putrescine added to the nutrient solution. Using metabolomics and proteomics analysis, we show that a significant part of the low-K response such as lower photosynthesis and N assimilation, is due to calcium and can be suppressed by low Ca conditions. Putrescine addition tends to restore photosynthesis and N assimilation but but aggravates the impact of low-K conditions on catabolism. We conclude that (i) effects of K deficiency can be partly alleviated by the use of low Ca and not only by K fertilization, and (ii) in addition to its role as a metabolite, putrescine participates in the regulation of the content in enzymes involved in carbon primary metabolism.
Several species of soil free-living saprotrophs can sometimes establish biotrophic symbiosis with plants, but the basic biology of this association remains largely unknown. Here, we investigate the symbiotic interaction between a common soil saprotroph, Clitopilus hobsonii (Agaricomycetes), and the American sweetgum (Liquidambar styraciflua). Notably, the colonized root cortical cells contain numerous microsclerotia-like structures. Fungal colonization led to increased plant growth and facilitated potassium uptake, particularly under potassium limitation (0.05 mM K+). The expression of plant genes related to potassium uptake is not altered during symbiosis, whereas the transcripts of three fungal genes encoding ACU, HAK, and SKC involved in K+ nutrition is found in colonized roots. We confirmed the K+ influx activities by expressing the ChACU and ChSKC genes into a yeast K+-uptake-defective mutant. Upregulation of the ChACU under 0.05 mM K+ and no K+ conditions was demonstrated in planta and in vitro compared to normal condition (5 mM K+). In addition, colonized plants displayed a larger accumulation of soluble sugars under 0.05 mM K+. The present study highlights that potassium limitation promotes this novel tree-fungus symbiosis mainly through a reciprocal transfer of additional carbon and potassium to both partners, and the role of dual soil saprotroph/symbiotroph in tree nutrition.
Embolism spreading in dehydrating angiosperm xylem is driven by gas movement between embolised and sap-filled conduits. Here, we examine how proximity to pre-existing embolism and hydraulic segmentation affect embolism propagation. Based on the optical method, we compared xylem embolism resistance between detached leaves and leaves attached to branches, and between intact leaves and leaves with cut minor veins for six species. Moreover, we directly compared the optical and pneumatic method on detached leaves. Embolism resistance of detached leaves was significantly lower than leaves attached to stems, except for two species with all vessels ending in their petioles. Cutting of minor veins showed limited embolism spreading in minor veins near the cuts prior to major veins. Moreover, there was strong agreement in embolism resistance between the optical and pneumatic method, with minor differences occurring during early stages of embolism formation. We conclude that embolism resistance may represent a relative trait, depending on the proximity and connectivity to pre-existing embolism as a gas source. Since embolism formation may not rely on a certain pressure difference threshold between functional and embolised conduits, we suggest that embolism is facilitated by pressure-driven gas diffusion, while hydraulic segmentation can prevent embolism propagation by reducing gas diffusion.
Nicotinamide-adenine dinucleotide (NAD) is involved in redox homeostasis and acts as a substrate for NADases, including poly (ADP-ribose) polymerases (PARPs) that add poly (ADP-ribose) polymers to proteins and DNA, and sirtuins that deacetylate proteins. Nicotinamide, a biproduct of NADases increases circadian period in both plants and animals. In mammals, the effect of nicotinamide on circadian period might be mediated by the PARPs and sirtuins because thy directly bind to core circadian oscillator genes. We have investigated whether PARPs and sirtuins contribute to the regulation of the circadian oscillator in Arabidopsis. We found no evidence that PARPs and sirtuins regulate the circadian oscillator of Arabidopsis or are involved in the response to nicotinamide. RNA-seq analysis indicated that PARPs regulate the expression of only a few genes, including FLOWERING LOCUS C. However, we found profound effects of reduced sirtuin 1 expression on gene expression during the day but not at night, and an embryo lethal phenotype in knockouts. Our results demonstrate that PARPS and sirtuins are not associated with NAD regulation of the circadian oscillator and that sirtuin 1 is associated with daytime regulation of gene expression.
ants share the phytobiome with other members of the ecological community by sharing their physiology. The phytobiome is a collective ecological entity that senses external and internal stimuli via its member’s sensing apparatus (senome). The activated senome generates intercellular, and intra- and inter-organismal signals that induce genetically and epigenetically dependent modifications of phytobiome member transcriptomes. Ultimately, these genetic modifications alter the phenotypes of the collective phytobiome members. Mycorrhiza, epiphytic fungi, and dodder can physically transfer signals between kin and non-kin plants. Phytobiome members can release infochemicals by themselves, or modify plant volatile emissions and root exudates to act as signals for plant–plant interactions. These signals can change plant physiology and induce holobiont updates in receiver plants via a facilitative or competitive mechanism. Receiver plants eavesdrop on phytobiome cues and signals to anticipate responses to unfolding challenges. An emerging body of information in plant–plant interactions through inter-kingdom communication can be exploited in integrated crop management under field conditions. However, a holistic view is crucial for the manipulation of complex systems, such as the phytobiome, to avoid potential butterfly effects.
Trees’ total amount of nonstructural carbohydrate (NSC) stores and the proportion of these stores residing as insoluble starch are vital traits for individuals living in variable environments. However, our understanding of how stores vary in response to environmental stress is poorly understood as the genetic component of storage is rarely accounted for in studies. Here, we quantified variation in NSC traits in branch samples taken from over 600 clonally transplanted black cottonwood (Populus trichocarpa) trees grown in two common gardens. We found heritable variation in both total NSC stores and the proportion of stores in starch (H2TNC = 0.19, H2PropStarch = 0.31), indicating a substantial genetic component of variation. In addition, we found high amounts of plasticity in both traits in response to cold temperatures and significant genotype-by-environment (GxE) interactions in the total amount of NSC stored (54% of P is GxE). This finding of high GxE indicates extensive variation across trees in their response to environment, which may explain why previous studies of carbohydrate stores’ responses to stress have failed to converge on a consistent pattern. Overall, we found high amounts of environmental and genetic variation in NSC storage concentrations, which may bolster species against future climate change.
Plant growth depends on the diurnal regulation of cellular processes, but it is not well understood if and how transcriptional regulation controls diurnal fluctuations at the protein-level. Here we report a high-resolution Arabidopsis thaliana (Arabidopsis) leaf rosette proteome acquired over a 12 h light : 12 h dark diurnal cycle and the phosphoproteome immediately before and after the light-to-dark and dark-to-light transitions. We quantified nearly 5000 proteins and 800 phosphoproteins, of which 288 fluctuated in their abundance and 226 fluctuated in their phosphorylation status. Of the phosphoproteins, 60% were quantified for changes in protein abundance. This revealed six proteins involved in nitrogen and hormone metabolism that had concurrent changes in both protein abundance and phosphorylation status. The diurnal proteome and phosphoproteome changes involve proteins in key cellular processes, including protein translation, light perception, photosynthesis, metabolism and transport. The phosphoproteome at the light-dark transitions revealed the dynamics at phosphorylation sites in either anticipation of or response to a change in light regime. Phosphorylation site motif analyses implicate casein kinase II and calcium/calmodulin dependent kinases among the primary light-dark transition kinases. The comparative analysis of the diurnal proteome and diurnal and circadian transcriptome established how mRNA and protein accumulation intersect in leaves during the diurnal cycle of the plant.
Flowering time is a major determinant of adaptation, fitness and yield in the allopolyploid species rapeseed (Brassica napus). Despite being a close relative to Arabidopsis thaliana, little is known about the timing of floral transition and which genes govern this process. Winter, semi-winter and spring type rapeseed have important life history characteristics that differ in vernalization requirements for flowering and are important for growing rapeseed in different regions of the world. In this study, we investigated the timing of vernalization-driven floral transition in winter rapeseed and the effect of photoperiod and developmental age on flowering time and vernalization responsiveness. Microscopy and whole transcriptome analysis at the shoot apical meristems of plants grown under controlled conditions showed that floral transition is initiated within few weeks of vernalization. Certain Bna.SOC1 and Bna.SPL5 homeologs were among the induced genes, suggesting that they are regulating the timing of cold-induced floral transition. Moreover, the flowering response of plants with shorter pre-vernalization period correlated with a delayed expression of Bna.SOC1 and Bna.SPL5 genes. In essence, this study presents a detailed analysis of vernalization-driven floral transition and the aspects of juvenility and dormancy and their effect on flowering time in rapeseed.
Circadian clocks have evolved to resonate with external day and night cycles. However, these entrainment signals are not consistent everywhere and vary with latitude, climate and seasonality. This leads to divergent selection for clocks which are locally adapted. To investigate the genetic basis for this circadian variation, we used a Delayed Fluorescence (DF) imaging assay to screen 191 naturally occurring Swedish Arabidopsis accessions for their circadian phenotypes. We demonstrate that period length co-varies with both geography and population sub-structure. Several candidate loci linked to period, phase and Relative Amplitude Error (RAE) were revealed by genome-wide association mapping and candidate genes were investigated using TDNA mutants. We show that natural variation in a single non-synonymous substitution within COR28 is associated with a long-period and late-flowering phenotype similar to that seen in TDNA knock-out mutants. COR28 is a known coordinator of flowering time, freezing tolerance and the circadian clock; all of which may form selective pressure gradients across Sweden. We demonstrate the effect of the COR28-58S SNP in increasing period length through a co-segregation analysis. Finally, we show that period phenotypic tails remain diverged under lower temperatures and follow a distinctive ‘arrow-shaped’ trend indicative of selection for a cold-biased temperature compensation response.
Capparis odoratissima is a tree species native to semi-arid environments of the northern coast of South America where low soil water availability coexists with frequent nighttime fog. A previous study showed that water applied to leaf surfaces enhanced leaf hydration, photosynthesis, and growth, but the mechanisms of foliar water uptake are unknown. Here we combine detailed anatomical evaluations with water and dye uptake experiments in the laboratory, and use immunolocalization of pectin and arabinogalactan protein epitopes to characterize water uptake pathways in leaves. Abaxially, the leaves of C. odoratissima are covered with peltate hairs, while the adaxial surfaces are glabrous. Both surfaces are able to absorb condensed water, but the lower surface has higher rates of water uptake. Numerous idioblasts connect the adaxial leaf surface and the abaxial peltate hairs, both of which contain hygroscopic substances such as arabinogalactan proteins and pectins. The highly specialized anatomy of the leaves of C odoratissima fulfills the dual function of minimizing water loss when stomata are closed, while maintaining the ability to absorb liquid water. Cell-wall related hygroscopic compounds in the peltate hairs and idioblasts create a network of microchannels that maintain leaf hydration and promote water uptake.
The heat tolerance of photosystem II (PSII) may promote carbon assimilation at higher temperatures and may help explain plant responses to climate change. PSII heat tolerance could lead to 1) increases in the high temperature compensation point (Tmax); 2) increases in the thermal breadth of photosynthesis (i.e. the photosynthetic Ω parameter) to promote a thermal generalist strategy of carbon assimilation; 3) increases in the optimum rate of carbon assimilation Popt and promote faster carbon assimilation; and/or 4) increases in the optimum temperature for photosynthesis (Topt). To address these hypotheses, we tested if the Tcrit, T50 and T95 metrics of PSII heat tolerance were correlated with each carbon assimilation parameter for 21 species. Hypothesis 1 was not supported, but we observed that T50 may estimate the upper thermal limit for Tmax at the species-level, and that community mean Tcrit may be useful for approximating Tmax. The T50 and T95 heat tolerance metrics were positively correlated with Ω in support of hypothesis 2. We found no support for hypotheses 3 or 4. Our study shows that high PSII heat tolerance is unlikely to improve carbon assimilation at higher temperatures, but may characterize thermal generalists with slow resource acquisition strategies.
Drought-related tree mortality is increasing globally, but the sequence of events leading to it remains poorly understood. To identify such sequence, we used a 2016 tree mortality event in the semi-arid pine forest of Yatir were dendrometry and sap flow measurements were carried out in 31 trees, of which seven died. A comparative analysis revealed three stages leading to mortality. First, a decrease in tree diameter in all dying trees, but not in the living ones, eight months ‘prior to the visual signs of mortality’ (PVSM; e.g., brown needles). Second, a decay to near zero in the diurnal stem swelling/shrinkage dynamics, reflecting the loss of stem radial water flow in the dying trees, six months PVSM. Third, cessation of stem sap flow three months PVSM. Eventual mortality could therefore be detected long before visual signs are observed, and the three stages identified here demonstrated the differential effects of drought on stem growth, water storage capabilities, and soil water uptake. The results indicated that breakdown of radial stem water flow and phloem functionality is a critical element in defining the ‘point of no return’ in the sequence of events leading to mortality of mature trees.
Plants alter their morphology and cellular homeostasis to promote resilience under a variety of heat regimes. Molecular processes that underlie these responses have been intensively studied and found to encompass diverse mechanisms operating across a broad range of cellular components, timescales and temperatures. This review explores recent progress throughout this landscape with a particular focus on thermosensing in plants. Direct temperature sensors include the photosensors phytochrome B and phototropin, the clock component ELF3 and an RNA switch. In addition, there are heat-regulated processes mediated by ion channels, lipids and lipid-modifying enzymes taking place at the plasma membrane and the chloroplast. In some cases the mechanism of temperature perception is well understood but in others this remains an open question. Potential novel thermosensing mechanisms are based on lipid and liquid phase separation. Finally, future research directions of high temperature perception and signalling pathways are discussed.
CONSTANS-LIKE (COL) family members are commonly implicated in light signal transduction during early photomorphogenesis. However, some of their functions remain unclear. Here, we propose a role for COL13 in hypocotyl elongation in Arabidopsis thaliana. We found that COL13 RNA accumulates at high levels in hypocotyls and that a disruption in the COL13 function via a T-DNA insertion or RNAi led to the formation of longer hypocotyls of Arabidopsis seedlings under red light. On the contrary, overexpression of COL13 resulted in the formation of shorter hypocotyls. Using various genetic, genomic, and biochemical assays, we proved that another COL protein, COL3, directly binds to the promoter of COL13, and the promoter region of COL3 was targeted by the transcription factor LONG HYPOCOTYL 5 (HY5), to form an HY5-COL3-COL13 regulatory chain for regulating hypocotyl elongation under red light. Additionally, further study demonstrated that COL13 interacts with COL3, and COL13 promotes the interaction between COL3 and CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1), suggesting a possible COP1-dependent COL3-COL13 feedback pathway. Our results provide new information regarding the gene network in mediating hypocotyl elongation.