Ectomycorrhizal symbiosis prepares its host locally and systemically for abiotic cue signaling.

Tree growth and survival are dependent on their ability to perceive signals, integrate them, and trigger timely and fitted molecular and growth responses. While ectomycorrhizal symbiosis is a predominant tree-microbe interaction in forest ecosystems, little is known about how and to what extent it helps trees cope with environmental changes. We hypothesized that the presence of Laccaria bicolor influences abiotic cue perception by Populus trichocarpa and the ensuing signaling cascade. We submitted ectomycorrhizal or non-ectomycorrhizal P. trichocarpa cuttings to short-term cessation of watering or ozone fumigation to focus on signaling networks before the onset of any physiological damage. Poplar gene expression, metabolite levels, and hormone levels were measured in several organs (roots, leaves, mycorrhizas) and integrated into networks. We discriminated the signal responses modified or maintained by ectomycorrhization. Ectomycorrhizas buffered hormonal changes in response to short-term environmental variations systemically prepared the root system for further fungal colonization and alleviated part of the root abscisic acid (ABA) signaling. The presence of ectomycorrhizas in the roots also modified the leaf multi-omics landscape and ozone responses, most likely through rewiring of the molecular drivers of photosynthesis and the calcium signaling pathway. In conclusion, P. trichocarpa-L. bicolor symbiosis results in a systemic remodeling of the host's signaling networks in response to abiotic changes. In addition, ectomycorrhizal, hormonal, metabolic, and transcriptomic blueprints are maintained in response to abiotic cues, suggesting that ectomycorrhizas are less responsive than non-mycorrhizal roots to abiotic challenges.

Changes in irradiance and vapour pressure deficit under drought induce distinct stomatal dynamics between glasshouse and field-grown poplars.

Recent research has shown that plant acclimation to diverse patterns of light intensity modifies the dynamics of their stomatal response. Therefore, whether plants are grown in controlled conditions or in the field may impact their stomatal dynamics. We analysed the stomatal dynamics of two Populus euramericana and two Populus nigra genotypes grown in the field under contrasting water availability. By comparing their stomatal dynamics with that of the same genotypes grown in a glasshouse, we were able to test whether differences between these growing conditions interacted with genotypic differences in affecting stomatal dynamics and responses to soil water deficit. We found that, despite higher stomatal density and smaller size, in the field stomatal dynamics were much slower than in the glasshouse. Overall, differences among genotypes and their response to soil water deficit were much less pronounced in the field compared with the glasshouse. These results indicate that stomatal dynamics are regulated by both genotype-specific and environmental factors. Moreover, having slower stomata may be advantageous under some conditions. While stomatal dynamics were linked with whole-plant transpiration per leaf area in both experiments, the contribution of stomatal morphology varies dependent on the environmental conditions.

Element content and expression of genes of interest in guard cells are connected to spatiotemporal variations in stomatal conductance.

Element content and expression of genes of interest on single cell types, such as stomata, provide valuable insights into their specific physiology, improving our understanding of leaf gas exchange regulation. We investigated how far differences in stomatal conductance (gs ) can be ascribed to changes in guard cells functioning in amphistomateous leaves. gs was measured during the day on both leaf sides, on well-watered and drought-stressed trees (two Populus euramericana Moench and two Populus nigra L. genotypes). In parallel, guard cells were dissected for element content and gene expressions analyses. Both were strongly arranged according to genotype, and drought had the lowest impact overall. Normalizing the data by genotype highlighted a structure on the basis of leaf sides and time of day both for element content and gene expression. Guard cells magnesium, phosphorus, and chlorine were the most abundant on the abaxial side in the morning, where gs was at the highest. In contrast, genes encoding H+ -ATPase and aquaporins were usually more abundant in the afternoon, whereas genes encoding Ca2+ -vacuolar antiporters, K+ channels, and ABA-related genes were in general more abundant on the adaxial side. Our work highlights the unique physiology of each leaf side and their analogous rhythmicity through the day.

Altered stomatal dynamics of two Euramerican poplar genotypes submitted to successive ozone exposure and water deficit.

The impact of ozone (O3) pollution events on the plant drought response needs special attention because spring O3 episodes are often followed by summer drought. By causing stomatal sluggishness, O3 could affect the stomatal dynamic during a subsequent drought event. In this context, we studied the impact of O3 exposure and water deficit (in the presence or in the absence of O3 episode) on the stomatal closure/opening mechanisms relative to irradiance or vapour pressure deficit (VPD) variation. Two genotypes of Populus nigra x deltoides were exposed to various treatments for 21 days. Saplings were exposed to 80 ppb/day O3 for 13 days, and then to moderate drought for 7 days. The curves of the stomatal response to irradiance and VPD changes were determined after 13 days of O3 exposure, and after 21 days in the case of subsequent water deficit, and then fitted using a sigmoidal model. The main responses under O3 exposure were stomatal closure and sluggishness, but the two genotypes showed contrasting responses. During stomatal closure induced by a change in irradiance, closure was slower for both genotypes. Nonetheless, the genotypes differed in stomatal opening under light. Carpaccio stomata opened more slowly than control stomata, whereas Robusta stomata tended to open faster. These effects could be of particular interest, as stomatal impairment was still present after O3 exposure and could result from imperfect recovery. Under water deficit alone, we observed slower stomatal closure in response to VPD and irradiance, but faster stomatal opening in response to irradiance, more marked in Carpaccio. Under the combined treatment, most of the parameters showed antagonistic responses. Our results highlight that it is important to take genotype-specific responses and interactive stress cross-talk into account to improve the prediction of stomatal conductance in response to various environmental modifications.

Altered stomatal dynamics induced by changes in irradiance and vapour-pressure deficit under drought: impacts on the whole-plant transpiration efficiency of poplar genotypes.

Recent findings were able to show significant variability of stomatal dynamics between species, but not much is known about factors influencing stomatal dynamics and its consequences on biomass production, transpiration and water-use efficiency (WUE). We assessed the dynamics of stomatal conductance (gs ) to a change of irradiance or vapour-pressure deficit (VPD) in two Populus euramericana and two Populus nigra genotypes grown under control and drought conditions. Our objectives were to determine the diversity of stomatal dynamics among poplar genotypes, and if soil water deficit can alter it. Physiological and morphological factors were investigated to find their potential links with stomatal morphology, WUE and its components at the whole-plant level. We found significant genotypic variability of gs dynamics to both irradiance and VPD. Genotypes with faster stomatal dynamics were correlated with higher stomatal density and smaller stomata, and the implications of these correlations are discussed. Drought slowed gs dynamics, depending on genotype and especially during stomatal closing. This finding is contrary to previous research on more drought-tolerant species. Independently of the treatment, faster stomatal dynamics were negatively correlated with daily whole-plant transpiration, presenting new evidence of a previously hypothesized contribution of stomatal dynamics to whole-plant water use.

Genes and gene clusters related to genotype and drought-induced variation in saccharification potential, lignin content and wood anatomical traits in Populus nigra.

Wood is a renewable resource that can be employed for the production of second generation biofuels by enzymatic saccharification and subsequent fermentation. Knowledge on how the saccharification potential is affected by genotype-related variation of wood traits and drought is scarce. Here, we used three Populus nigra L. genotypes from habitats differing in water availability to (i) investigate the relationships between wood anatomy, lignin content and saccharification and (ii) identify genes and co-expressed gene clusters related to genotype and drought-induced variation in wood traits and saccharification potential. The three poplar genotypes differed in wood anatomy, lignin content and saccharification potential. Drought resulted in reduced cambial activity, decreased vessel and fiber lumina, and increased the saccharification potential. The saccharification potential was unrelated to lignin content as well as to most wood anatomical traits. RNA sequencing of the developing xylem revealed that 1.5% of the analyzed genes were differentially expressed in response to drought, while 67% differed among the genotypes. Weighted gene correlation network analysis identified modules of co-expressed genes correlated with saccharification potential. These modules were enriched in gene ontology terms related to cell wall polysaccharide biosynthesis and modification and vesicle transport, but not to lignin biosynthesis. Among the most strongly saccharification-correlated genes, those with regulatory functions, especially kinases, were prominent. We further identified transcription factors whose transcript abundances differed among genotypes, and which were co-regulated with genes for biosynthesis and modifications of hemicelluloses and pectin. Overall, our study suggests that the regulation of pectin and hemicellulose metabolism is a promising target for improving wood quality of second generation bioenergy crops. The causal relationship of the identified genes and pathways with saccharification potential needs to be validated in further experiments.