The multiple roles of trichomes in two Croton species.

Trichomes are common in plants from dry environments, and despite their recognized role in protection and defense, little is known about their role as absorptive structures and in other aspects of leaf ecophysiology. We combine anatomical and ecophysiological data to evaluate how trichomes affect leaf gas exchange and water balance during drought. We studied two congeneric species with pubescent leaves which co-occur in Brazilian Caatinga: Croton blanchetianus (dense trichomes) and Croton adenocalyx (sparse trichomes). We found a novel foliar water uptake (FWU) pathway in C. blanchetianus composed of stellate trichomes and underlying epidermal cells and sclereids that interconnect the trichomes from both leaf surfaces. The water absorbed by these trichomes is redistributed laterally by pectin protuberances on mesophyll cell walls. This mechanism enables C. blanchetianus leaves to absorb water more efficiently than C. adenocalyx. Consequently, the exposure of C. blanchetianus to dew during drought improved its leaf gas exchange and water status more than C. adenocalyx. C. blanchetianus trichomes also increase their leaf capacity to reflect light and maintain lower temperatures during drought. Our results emphasize the multiple roles that trichomes might have on plant functioning and the importance of FWU for the ecophysiology of Caatinga plants during drought.

Importance of hydraulic strategy trade-offs in structuring response of canopy trees to extreme drought in central Amazon.

Plant ecophysiological trade-offs between different strategies for tolerating stresses are widely theorized to shape forest functional diversity and vulnerability to climate change. However, trade-offs between hydraulic and stomatal regulation during natural droughts remain under-studied, especially in tropical forests. We investigated eleven mature forest canopy trees in central Amazonia during the strong 2015 El Niño. We found greater xylem embolism resistance ([Formula: see text] = - 3.3 ± 0.8 MPa) and hydraulic safety margin (HSM = 2.12 ± 0.57 MPa) than previously observed in more precipitation-seasonal rainforests of eastern Amazonia and central America. We also discovered that taller trees exhibited lower embolism resistance and greater stomatal sensitivity, a height-structured trade-off between hydraulic resistance and active stomatal regulation. Such active regulation of tree water status, triggered by the onset of stem embolism, acted as a feedback to avoid further increases in embolism, and also explained declines in photosynthesis and transpiration. These results suggest that canopy trees exhibit a conservative hydraulic strategy to endure drought, with trade-offs between investment in xylem to reduce vulnerability to hydraulic failure, and active stomatal regulation to protect against low water potentials. These findings improve our understanding of strategies in tropical forest canopies and contribute to more accurate prediction of drought responses.

Asymbiotic nitrogen fixation in the phyllosphere of the Amazon forest: Changing nitrogen cycle paradigms.

Biological nitrogen fixation is a key process for the maintenance of natural ecosystems productivity. In tropical forests, the contribution of asymbiotic nitrogen fixation (ANF) to the nitrogen (N) input has been underestimated, even though few studies have shown that ANF may be as important as symbiotic nitrogen fixation in such environments. The inputs and abiotic modulators of ANF in the Amazon forest are not completely understood. Here, we determined ANF rates and estimated the N inputs from ANF in the phyllosphere, litter and rhizospheric soil of nine tree species in the Amazon forest over time, including an extreme drought period induced by the El Niño-Southern Oscillation. Our data showed that ANF rates in the phyllosphere were 2.8- and 17.6-fold higher than in the litter and rhizospheric soil, respectively, and was highly dependent on tree taxon. Sampling time was the major factor modulating ANF in all forest compartments. At the driest period, ANF rates were approximately 1.8-fold and 13.1-fold higher than at periods with higher rainfall, before and after the extreme drought period, respectively. Tree species was a key modulator of ANF in the phyllosphere, as well as N and Vanadium concentrations. Carbon, molybdenum and vanadium concentrations were significant modulators of ANF in the litter. Based on ANF rates at the three sampling times, we estimated that the N input in the Amazon forest through ANF in the phyllosphere, litter and rhizospheric soil, was between 0.459 and 0.714 kg N ha-1 yr-1. Our results highlight the importance of ANF in the phyllosphere for the N input in the Amazon forest, and suggest that changes in the patterns of ANF driven by large scale climatic events may impact total N inputs and likely alter forest productivity.

Costs and benefits of gas inside wood and its relationship with anatomical traits: a contrast between trees and lianas.

Gas inside wood plays an important role in plant functioning, but there has been no study examining the adaptive nature of gas inside wood across plants differing in biomechanical demands. Using a comparative approach, we measured gas volumetric content, xylem's anatomical traits and wood density of 15 tree and 16 liana species, to test whether gas content varies between these plant types strongly differing in their biomechanical demands. We asked (i) whether trees and lianas differ in gas content and (ii) how anatomical traits and wood density are related to gas content. Lianas had significantly less gas content in their branches compared with tree species. In tree species, gas content scaled positively with fiber, vessel and xylem cross-sectional area and fiber and vessel diameter, and negatively with dry-mass density. When pooling trees and lianas together, fiber cross-sectional area was the strongest predictor of gas content, with higher xylem cross-sectional area of fiber associated with higher gas content. In addition, we showed, through a simple analytical model, that gas inside wood increases the minimum branch diameter needed to prevent rupture, and this effect was stronger on trees compared with lianas. Our results support the view that gas inside wood plays an important role in the evolution of biomechanical functioning in different plant forms. Gas inside wood may also play an important role in physiological activities such as water transport, storage, photosynthesis and respiration, but it is still unknown whether these roles are or are not secondary to the mechanical support.

Molecular responses to freshwater limitation in the mangrove tree Avicennia germinans (Acanthaceae).

Environmental variation along the geographical space can shape populations by natural selection. In the context of global warming and changing precipitation regimes, it is crucial to understand the role of environmental heterogeneity in tropical trees adaptation, given their disproportional contribution to water and carbon biogeochemical cycles. Here, we investigated how heterogeneity in freshwater availability along tropical wetlands has influenced molecular variations of the black mangrove (Avicennia germinans). A total of 57 trees were sampled at seven sites differing markedly in precipitation regime and riverine freshwater inputs. Using 2,297 genome-wide single nucleotide polymorphic markers, we found signatures of natural selection by the association between variations in allele frequencies and environmental variables, including the precipitation of the warmest quarter and the annual precipitation. Additionally, we found candidate loci for selection based on statistical deviations from neutral expectations of interpopulation differentiation. Most candidate loci within transcribed sequences were functionally associated with central aspects of drought tolerance or plant response to drought. Moreover, our results suggest the occurrence of the rapid evolution of a population, probably in response to sudden and persistent limitations in plant access to soil water, following a road construction in 1974. Observations supporting rapid evolution included the reduction in tree size and changes in allele frequencies and in transcript expression associated with increased drought tolerance through the accumulation of osmoprotectants and antioxidants, biosynthesis of cuticles, protection against protein degradation, stomatal closure, photorespiration and photosynthesis. We describe a major role of spatial heterogeneity in freshwater availability in the specialization of this typically tropical tree.

Local adaptation of a dominant coastal tree to freshwater availability and solar radiation suggested by genomic and ecophysiological approaches.

Local adaptation is often a product of environmental variations in geographical space and has implications for biodiversity conservation. We investigated the role of latitudinal heterogeneity in climate on the organization of genetic and phenotypic variation in the dominant coastal tree Avicennia schaueriana. In a common garden experiment, samples from an equatorial region, with pronounced seasonality in precipitation, accumulated less biomass, and showed lower stomatal conductance and transpiration, narrower xylem vessels, smaller leaves and higher reflectance of long wavelengths by the stem epidermis than samples from a subtropical region, with seasonality in temperature and no dry season. Transcriptomic differences identified between trees sampled under field conditions at equatorial and subtropical sites, were enriched in functional categories such as responses to temperature, solar radiation, water deficit, photosynthesis and cell wall biosynthesis. Remarkably, the diversity based on genome-wide SNPs revealed a north-south genetic structure and signatures of selection were identified for loci associated with photosynthesis, anthocyanin accumulation and the responses to osmotic and hypoxia stresses. Our results suggest the existence of divergence in key resource-use characteristics, likely driven by seasonality in water deficit and solar radiation. These findings provide a basis for conservation plans and for predicting coastal plants responses to climate change.

Microbiomes of Velloziaceae from phosphorus-impoverished soils of the campos rupestres, a biodiversity hotspot.

The rocky, seasonally-dry and nutrient-impoverished soils of the Brazilian campos rupestres impose severe growth-limiting conditions on plants. Species of a dominant plant family, Velloziaceae, are highly specialized to low-nutrient conditions and seasonal water availability of this environment, where phosphorus (P) is the key limiting nutrient. Despite plant-microbe associations playing critical roles in stressful ecosystems, the contribution of these interactions in the campos rupestres remains poorly studied. Here we present the first microbiome data of Velloziaceae spp. thriving in contrasting substrates of campos rupestres. We assessed the microbiomes of Vellozia epidendroides, which occupies shallow patches of soil, and Barbacenia macrantha, growing on exposed rocks. The prokaryotic and fungal profiles were assessed by rRNA barcode sequencing of epiphytic and endophytic compartments of roots, stems, leaves and surrounding soil/rocks. We also generated root and substrate (rock/soil)-associated metagenomes of each plant species. We foresee that these data will contribute to decipher how the microbiome contributes to plant functioning in the campos rupestres, and to unravel new strategies for improved crop productivity in stressful environments.

Nitrogen dynamics in subtropical fringe and basin mangrove forests inferred from stable isotopes.

Mangroves exhibit low species richness compared to other tropical forests, but great structural and functional diversity. Aiming to contribute to a better understanding of the functioning of mangrove forests, we investigated nitrogen (N) dynamics in two physiographic types of mangroves (fringe and basin forests) in southeastern Brazil. Because fringe forests are under great influence of tidal flushing we hypothesized that these forests would exhibit higher N cycling rates in sediment and higher N losses to the atmosphere compared to basin forests. We quantified net N mineralization and nitrification rates in sediment and natural abundance of N stable isotopes (δ15N) in the sediment-plant-litter system. The fringe forest exhibited higher net N mineralization rates and δ15N in the sediment-plant-litter system, but net nitrification rates were similar to those of the basin forest. The results of the present study suggest that fringe forests exhibit higher N availability and N cycling in sediment compared to basin forests.

Trade-off between soluble protein production and nutritional storage in Bromeliaceae.

BACKGROUND AND AIMS: Bromeliads are able to occupy some of the most nutrient-poor environments especially because they possess absorptive leaf trichomes, leaves organized in rosettes, distinct photosynthetic pathways [C3, Crassulacean acid metabolism (CAM) or facultative C3-CAM], and may present an epiphytic habit. The more derived features related to these traits are described for the Tillandsioideae subfamily. In this context, the aims of this study were to evaluate how terrestrial predators contribute to the nutrition and performance of bromeliad species, subfamilies and ecophysiological types, whether these species differ in their ecophysiological traits and whether the physiological outcomes are consistent among subfamilies and types (e.g. presence/absence of tank, soil/tank/atmosphere source of nutrients, trichomes/roots access to nutrients). METHODS: Isotopic (15N-enriched predator faeces) and physiological methods (analyses of plant protein, amino acids, growth, leaf mass per area and total N incorporated) in greenhouse experiments were used to investigate the ecophysiological contrasts between Tillandsioideae and Bromelioideae, and among ecophysiological types when a predatory anuran contributes to their nutrition. KEY RESULTS: It was observed that Bromelioideae had higher concentrations of soluble protein and only one species grew more (Ananas bracteatus), while Tillandsioideae showed higher concentrations of total amino acids, asparagine and did not grow. The ecophysiological types that showed similar protein contents also had similar growth. Additionally, an ordination analysis showed that the subfamilies and ecophysiological types were discrepant considering the results of the total nitrogen incorporated from predators, soluble protein and asparagine concentrations, relative growth rate and leaf mass per area. CONCLUSIONS: Bromeliad subfamilies showed a trade-off between two strategies: Tillandsioideae stored nitrogen into amino acids possibly for transamination reactions during nutritional stress and did not grow, whereas Bromelioideae used nitrogen for soluble protein production for immediate utilization, possibly for fast growth. These results highlight that Bromeliaceae evolution may be directly associated with the ability to stock nutrients.

Fine root biomass and root length density in a lowland and a montane tropical rain forest, SP, Brazil / Biomassa de raízes finas e densidade do comprimento radicular em uma floresta tropical chuvosa de terras baixas e montana, SP, Brasil

Fine roots, <2 mm in diameter, are responsible for water and nutrient uptake and therefore have a central role in carbon, nutrient and water cycling at the plant and ecosystem level. The root length density (RLD), fine root biomass (FRB) and vertical fine root distribution (VRD) in the soil profile have been used as good descriptors of resource-use efficiency and carbon storage in the soil. Along altitudinal gradients, decreases in temperature and radiation inputs (depending on the frequency of fog events) may reduce decomposition rates and nutrient availability what might stimulate plants to invest in fine roots, increasing acquisition of resources. We evaluated the seasonal variation of fine root parameters in a Lowland and Montane forest at the Atlantic Rain Forest. We hypothesized that, due to lower decomposition rates at the Montane site, the FRB and RLD at soil surface will be higher in this altitude, which can maximize the efficiency of resource absorption. FRB and RLD were higher in the Montane forest in both seasons, especially at the 0-5 layer. At the 0-5 soil layer in both sites, RLD increased from dry to wet season independently of variations in FRB. Total FRB in the top 30 cm of the soil at the Lowland site was significantly lower (334 g.m-2 in the dry season and 219 g.m-2 in the wet season) than at the Montane forest (875 and 451 g.m-2 in the dry and wet season, respectively). In conclusion, despite the relevance of FRB to describe processes related to carbon dynamics, the variation of RLD between seasons, independently of variations in FRB, indicates that RLD is a better descriptor for studies characterizing the potential of water and nutrient uptake at the Atlantic Rain Forest. The differences in RLD between altitudes within the context of resource use should be considered in studies about plant establishment, seedling growth and population dynamics at the Atlantic Rain Forest. At the ecosystem level, RLD and it seasonal variations may improve our understanding of the Atlantic rain forest functioning in terms of the biogeochemical fluxes in a possible scenario of climate change and environmental changes.

Raízes finas, <2 mm de diâmetro, são as principais responsáveis pela absorção de água e nutrientes e, portanto, têm um papel central nos ciclos carbono, água e nutrientes, desde o nível da planta até o ecossistêmico. A densidade do comprimento radicular (DCR), a biomassa de raízes finas (BRF) e a distribuição vertical de raízes finas (DVR) no perfil do solo têm sido utilizados como bons descritores da eficiência no uso de recursos e de estocagem de carbono no solo. Ao longo de gradientes altitudinais, a diminuição da temperatura e da radiação solar (dependendo da frequência de eventos de neblina) podem reduzir as taxas de decomposição e disponibilidade de nutrientes, o que poderia estimular o aumento do investimento das raízes finas para maximizar a absorção de água e nutrientes. O presente estudo avaliou a variação sazonal de parâmetros radiculares nas florestas ombrófilas densas de Terras Baixas (FODTB) e Montana (FODM) na Mata Atlântica. A hipótese foi a de que o investimento em BRF e DCR seria maior na FODM, o que poderia maximizar a eficiência na absorção de recursos. A BRF e a DCR foram maiores na FODM em ambas as estações, especialmente na profundidade de 0-5 cm. A BRF total nos primeiros 30 cm de solo na FODTB foi significativamente menor (334 g.m-2 na estação seca e 219 g.m-2 na chuvosa) do que na FODM (875 e 451 g.m-2 nas estações seca e chuvosa, respectivamente). Na profundidade de 0-5 cm em ambas as altitudes, a DCR aumentou da estação seca para chuvosa independentemente de variações na BRF. Apesar da relevância da BRF para descrever processos relacionados à dinâmica de carbono, a variação da DCR entre estações, independente de variações na BRF, indica que a DCR é um melhor descritor para estudos caracterizando o potencial de absorção de água e nutrientes na Floresta Atlântica. As diferenças da DCR entre altitudes dentro do contexto de uso de recursos devem ser consideradas em estudos sobre estabelecimento, crescimento de plântulas e dinâmica de populações na Floresta Atlântica. No nível ecossistêmico, as variações sazonais da DCR podem aumentar nosso entendimento sobre o funcionamento da Floresta Atlântica em termos de fluxos biogeoquímicos em um possível cenário de mudanças climáticas e ambientais.