On a Cold Night: Transcriptomics of Grapevine Flower Unveils Signal Transduction and Impacted Metabolism.

Low temperature is a critical environmental factor limiting plant productivity, especially in northern vineyards. To clarify the impact of this stress on grapevine flower, we used the Vitis array based on Roche-NimbleGen technology to investigate the gene expression of flowers submitted to a cold night. Our objectives were to identify modifications in the transcript levels after stress and during recovery. Consequently, our results confirmed some mechanisms known in grapes or other plants in response to cold stress, notably, (1) the pivotal role of calcium/calmodulin-mediated signaling; (2) the over-expression of sugar transporters and some genes involved in plant defense (especially in carbon metabolism), and (3) the down-regulation of genes encoding galactinol synthase (GOLS), pectate lyases, or polygalacturonases. We also identified some mechanisms not yet known to be involved in the response to cold stress, i.e., (1) the up-regulation of genes encoding G-type lectin S-receptor-like serine threonine-protein kinase, pathogen recognition receptor (PRR5), or heat-shock factors among others; (2) the down-regulation of Myeloblastosis (MYB)-related transcription factors and the Constans-like zinc finger family; and (3) the down-regulation of some genes encoding Pathogen-Related (PR)-proteins. Taken together, our results revealed interesting features and potentially valuable traits associated with stress responses in the grapevine flower. From a long-term perspective, our study provides useful starting points for future investigation.

Cold-night responses in grapevine inflorescences.

Cold nights impact grapevine flower development and fruit set. Regulation at the female meiosis stepmay be of considerable importance for further understanding on how flower reacts to cold stress. In this study, the impact of chilling temperature (0 °C overnight) on carbon metabolism was investigated in the inflorescencesof two cultivars, Pinot noir (Pinot) and Gewurztraminer (Gewurtz.). Fluctuations in photosynthetic activity and carbohydrate metabolism were monitored by analyzing gas exchanges, simultaneous photosystem I and II activities, andcarbohydrate content. Further, the expression of PEPc, PC, FNR, ISO, OXO, AGPase, amylases and invertase genes, activities of various enzymes, as well as metabolomic analysis were attained. Results showed that the chilling night has different impacts depending on cultivars. Thus, in Gewurtz., net photosynthesis (Pn) was transiently increased whereas, in Pinot, the Pn increase was persistent and concomitant with an inhibition of respiration. However, during the days following the cold night, photosynthetic activity was decreased, and the cyclic electron flow was inhibited in Gewurtz., suggesting lower efficient energy dissipation. Likewise, metabolomic analysis revealed that several metabolites contents (namely alanine, GABA, lysine and succinate)were distinctly modulated in the two cultivars. Taking together, these results reflect a photosynthetic metabolism alteration or internal CO2 conductance in Gewurtz. explaining partly why Pinot is less susceptible to cold stress.

Cross-talk between environmental stresses and plant metabolism during reproductive organ abscission.

In plants, flowering is a crucial process for reproductive success and continuity of the species through time. Fruit production requires the perfect development of reproductive structures. Abscission, a natural process, can occur to facilitate shedding of no longer needed, infected, or damaged organs. If stress occurs during flower development, abscission can intervene at flower level, leading to reduced yield. Flower abscission is a highly regulated developmental process simultaneously influenced and activated in response to exogenous (changing environmental conditions, interactions with microorganisms) and endogenous (physiological modifications) stimuli. During climate change, plant communities will be more susceptible to environmental stresses, leading to increased flower and fruit abscission, and consequently a decrease in fruit yield. Understanding the impacts of stress on the reproductive phase is therefore critical for managing future agricultural productivity. Here, current knowledge on flower/fruit abscission is summarized by focusing specifically on effects of environmental stresses leading to this process in woody plants. Many of these stresses impair hormonal balance and/or carbohydrate metabolism, but the exact mechanisms are far from completely known. Hormones are the abscission effectors and the auxin/ethylene balance is of particular importance. The carbohydrate pathway is the result of complex regulatory processes involving the balance between photosynthesis and mobilization of reserves. Hormones and carbohydrates together participate in complex signal transduction systems, especially in response to stress. The available data are discussed in relation to reproductive organ development and the process of abscission.

Distinct regulation in inflorescence carbohydrate metabolism according to grapevine cultivars during floral development.

Carbohydrate metabolism is important in plant sexual reproduction because sugar contents are determining factors for both flower initiation and floral organ development. In woody plants, flowering represents the most energy-consuming step crucial to reproductive success. Nevertheless, in these species, the photosynthesis performed by flowers supplies the carbon required for reproduction. In grapevine (Vitis vinifera), the inflorescence has a specific status because this organ imports carbohydrates at the same time as it exports photoassimilates. In this study, fluctuations in carbohydrate metabolism were monitored by analyzing gas exchanges, photosynthetic electron transport capacity, carbohydrate contents and some activities of carbohydrate metabolism enzymes, in the inflorescences of Pinot noir and Gewurztraminer, two cultivars with a different sensitivity to coulure phenomenon. Our results showed that photosynthetic activity and carbohydrate metabolism are clearly different and differently regulated during the floral development in the two cultivars. Indeed, the regulation of the linear electron flow and the cyclic electron flow is not similar. Moreover, the regulation of PSII activity, with a higher Y(NPQ)/Y(NO) ratio in Gewurztraminer, can be correlated with the higher protection of the photosynthetic chain and consequently with the higher yield under optimal conditions of this cultivar. At least, our results showed a higher photosynthetic activity and a better protection of PSI in Pinot noir during the floral development.

Adaptation of grapevine flowers to cold involves different mechanisms depending on stress intensity.

Grapevine flower development and fruit set are influenced by cold nights in the vineyard. To investigate the impact of cold stress on carbon metabolism in the inflorescence, we exposed the inflorescences of fruiting cuttings to chilling and freezing temperatures overnight and measured fluctuations in photosynthesis and sugar content. Whatever the temperature, after the stress treatment photosynthesis was modified in the inflorescence, but the nature of the alteration depended on the intensity of the cold stress. At 4°C, photosynthesis in the inflorescence was impaired through non-stomatal limitations, whereas at 0°C it was affected through stomatal limitations. A freezing night (-3°C) severely deregulated photosynthesis in the inflorescence, acting primarily on photosystem II. Cold nights also induced accumulation of sugars. Soluble carbohydrates increased in inflorescences exposed to -3°C, 0°C and 4°C, but starch accumulated only in inflorescences of plants treated at 0 and -3°C. These results suggest that inflorescences are able to cope with cold temperatures by adapting their carbohydrate metabolism using mechanisms that are differentially induced according to stress intensity.