Involvement of aquaporins on nitrogen-acquisition strategies of juvenile and adult plants of an epiphytic tank-forming bromeliad.

MAIN CONCLUSION: Depending on the N source and plant ontogenetic state, the epiphytic tank-forming bromeliad Vriesea gigantea can modulate aquaporin expression to maximize the absorption of the most available nitrogen source. Epiphytic bromeliads frequently present a structure formed by the overlapping of leaf bases where water and nutrients can be accumulated and absorbed, called tank. However, this structure is not present during the juvenile ontogenetic phase, leading to differences in nutrient acquisition strategies. Recent studies have shown a high capacity of the bromeliad Vriesea gigantea, an epiphytic tank-forming bromeliad, to absorb urea by their leaves. Since plant aquaporins can facilitate the diffusion of urea through the membranes, we cloned three foliar aquaporin genes, VgPIP1;1, VgPIP1;2 and VgTIP2;1 from V. gigantea plants. Through functional studies, we observed that besides water, VgTIP2;1 was capable of transporting urea while VgPIP1;2 may facilitate ammonium/ammonia diffusion. Moreover, aiming at identifying urea and ammonium-induced changes in aquaporin expression in leaves of juvenile and adult-tank plants, we showed that VgPIP1;1 and VgPIP1;2 transcripts were up-regulated in response to either urea or ammonium only in juvenile plants, while VgTIP2;1 was up-regulated in response to urea only in adult-tank plants. Thereby, an ontogenetic shift from juvenile to adult-tank-forming-plant appears to occur with metabolic changes regarding nitrogen metabolism regulation. Investigating urea metabolism in wild species that naturally cope with organic N sources, such as V. gigantea, may provide the knowledge to modify nitrogen use efficiency of crop plants.

The carbon bonus of organic nitrogen enhances nitrogen use efficiency of plants.

The importance of organic nitrogen (N) for plant nutrition and productivity is increasingly being recognized. Here we show that it is not only the availability in the soil that matters, but also the effects on plant growth. The chemical form of N taken up, whether inorganic (such as nitrate) or organic (such as amino acids), may significantly influence plant shoot and root growth, and nitrogen use efficiency (NUE). We analysed these effects by synthesizing results from multiple laboratory experiments on small seedlings (Arabidopsis, poplar, pine and spruce) based on a tractable plant growth model. A key point is that the carbon cost of assimilating organic N into proteins is lower than that of inorganic N, mainly because of its carbon content. This carbon bonus makes it more beneficial for plants to take up organic than inorganic N, even when its availability to the roots is much lower - up to 70% lower for Arabidopsis seedlings. At equal growth rate, root:shoot ratio was up to three times higher and nitrogen productivity up to 20% higher for organic than inorganic N, which both are factors that may contribute to higher NUE in crop production.

Patterns of plant biomass partitioning depend on nitrogen source.

Nitrogen (N) availability is a strong determinant of plant biomass partitioning, but the role of different N sources in this process is unknown. Plants inhabiting low productivity ecosystems typically partition a large share of total biomass to belowground structures. In these systems, organic N may often dominate plant available N. With increasing productivity, plant biomass partitioning shifts to aboveground structures, along with a shift in available N to inorganic forms of N. We tested the hypothesis that the form of N taken up by plants is an important determinant of plant biomass partitioning by cultivating Arabidopsis thaliana on different N source mixtures. Plants grown on different N mixtures were similar in size, but those supplied with organic N displayed a significantly greater root fraction. ¹5N labelling suggested that, in this case, a larger share of absorbed organic N was retained in roots and split-root experiments suggested this may depend on a direct incorporation of absorbed amino acid N into roots. These results suggest the form of N acquired affects plant biomass partitioning and adds new information on the interaction between N and biomass partitioning in plants.

Specific leaf areas of the tank bromeliad Guzmania monostachia perform distinct functions in response to water shortage.

Leaves comprise most of the vegetative body of tank bromeliads and are usually subjected to strong longitudinal gradients. For instance, while the leaf base is in contact with the water accumulated in the tank, the more light-exposed middle and upper leaf sections have no direct access to this water reservoir. Therefore, the present study attempted to investigate whether different leaf portions of Guzmania monostachia, a tank-forming C(3)-CAM bromeliad, play distinct physiological roles in response to water shortage, which is a major abiotic constraint in the epiphytic habitat. Internal and external morphological features, relative water content, pigment composition and the degree of CAM expression were evaluated in basal, middle and apical leaf portions in order to allow the establishment of correlations between the structure and the functional importance of each leaf region. Results indicated that besides marked structural differences, a high level of functional specialization is also present along the leaves of this bromeliad. When the tank water was depleted, the abundant hydrenchyma of basal leaf portions was the main reservoir for maintaining a stable water status in the photosynthetic tissues of the apical region. In contrast, the CAM pathway was intensified specifically in the upper leaf section, which is in agreement with the presence of features more suitable for the occurrence of photosynthesis at this portion. Gas exchange data indicated that internal recycling of respiratory CO(2) accounted for virtually all nighttime acid accumulation, characterizing a typical CAM-idling pathway in the drought-exposed plants. Altogether, these data reveal a remarkable physiological complexity along the leaves of G. monostachia, which might be a key adaptation to the intermittent water supply of the epiphytic niche.

Microbial activities and foliar uptake of nitrogen in the epiphytic bromeliad Vriesea gigantea.

In contrast to terrestrial plants, epiphytic tank bromeliads take up nutrients mainly over their tank leaf surface. The form in which nutrients are available in the tanks is determined by the source and the complex interplay between tank microbes, which transform them and the epiphytes that take them up. To elucidate the importance of different nitrogenous compounds for the nitrogen (N) nutrition of Vriesea gigantea from the Atlantic Rainforest, Brazil, N transformation processes in tank water as well as foliar uptake rates were estimated by 15N labelling techniques. Microorganisms actively transformed N compounds in the tank. Specifically, organic N compounds were rapidly mineralized to NH4+, while nitrification was negligible. Plants took up both organic and inorganic N forms, with a clear preference for NH4+. NH4+ comprised the largest and, because of fast mineralization rates, the most constant dissolved N pool in the tank water. Excretion of ureases by the plants together with an unusual uptake kinetic for urea also suggests that urea may be potentially important as an N source.