Alessio Giovannelli

Intra-annual dynamics of non-structural carbohydrates in the cambium of mature conifer trees reflects radial growth demands

The presence of soluble carbohydrates in the cambial zone, either from sugars recently produced during photosynthesis or from starch remobilized from storage organs, is necessary for radial tree growth. However, considerable uncertainties on carbohydrate dynamics and the consequences on tree productivity exist. This study aims to better understand the variation in different carbon pools at intra-annual resolution by quantifying how cambial zone sugar and starch concentrations fluctuate over the season and in relation to cambial phenology. A comparison between two physiologically different species growing at the same site, i.e., the evergreen Picea abies Karst. and the deciduous Larix decidua Mill., and between L. decidua from two contrasting elevations, is presented to identify mechanisms of growth limitation. Results indicate that the annual cycle of sugar concentration within the cambial zone is coupled to the process of wood formation. The highest sugar concentration is observed when the number of cells in secondary wall formation and lignification stages is at a maximum, subsequent to most radial growth. Starch disappears in winter, while other freeze-resistant non-structural carbohydrates (NSCs) increase. Slight differences in NSC concentration between species are consistent with the differing climate sensitivity of the evergreen and deciduous species investigated. The general absence of differences between elevations suggests that the cambial activity of trees growing at the treeline was not limited by the availability of carbohydrates at the cambial zone but instead by environmental controls on the growing season duration.

Impact of warming and drought on carbon balance related to wood formation in black spruce

BACKGROUND AND AIMS Wood formation in trees represents a carbon sink that can be modified in the case of stress. The way carbon metabolism constrains growth during stress periods (high temperature and water deficit) is now under debate. In this study, the amounts of non-structural carbohydrates (NSCs) for xylogenesis in black spruce, Picea mariana, saplings were assessed under high temperature and drought in order to determine the role of sugar mobilization for osmotic purposes and its consequences for secondary growth. METHODS Four-year-old saplings of black spruce in a greenhouse were subjected to different thermal conditions with respect to the outside air temperature (T0) in 2010 (2 and 5 °C higher than T0) and 2011 (6 °C warmer than T0 during the day or night) with a dry period of about 1 month in June of each year. Wood formation together with starch, NSCs and leaf parameters (water potential and photosynthesis) were monitored from May to September. KEY RESULTS With the exception of raffinose, the amounts of soluble sugars were not modified in the cambium even if gas exchange and photosynthesis were greatly reduced during drought. Raffinose increased more than pinitol under a pre-dawn water potential of less than -1 Mpa, presumably because this compound is better suited than polyol for replacing water and capturing free radicals, and its degradation into simple sugar is easier. Warming decreased the starch storage in the xylem as well the available hexose pool in the cambium and the xylem, probably because of an increase in respiration. CONCLUSIONS Radial stem growth was reduced during drought due to the mobilization of NSCs for osmotic purposes and due to the lack of cell turgor. Thus plant water status during wood formation can influence the NSCs available for growth in the cambium and xylem.

Transcriptome changes in the cambial region of poplar (Populus alba L.) in response to water deficit

A transcriptome analysis of the Populus alba cambial region was performed with the aim of elucidating the gene network underlying the response to water deficit within the cambium and differentiating derivative cambial cells. Water stress was induced in 1-year-old P. alba plants by withholding water for 9 days. At that time, leaf predawn water potential fell to -0.8 MPa, resulting in a significant reduction in stomatal conductance, CO(2) assimilation and a consistent increment of stem shrinkage. These effects were almost fully reversed by re-hydration. The water deficit resulted in changes in gene expression that affected several functional categories, such as protein metabolism, cell wall metabolism, stress response, transporters and transcriptional regulation. The function of up- and down-regulated genes is discussed considering the physiological response of the plants to water deficit.

Hormonal signals involved in the regulation of cambial activity, xylogenesis and vessel patterning in trees.

The radial growth of plant stem is based on the development of cribro-vascular cambium tissues. It affects the transport efficiency of water, mineral nutrients and photoassimilates and, ultimately, also plant height. The rate of cambial cell divisions for the assembly of new xylem and phloem tissue primordia and the rate of differentiation of the primordia into mature tissues determine the amount of biomass produced and, in the case of woody species, the wood quality. These complex physiological processes proceed at a rate which depends on several factors, acting at various levels: growth regulators, resource availability and environmental factors. Several hormonal signals and, more recently, further regulatory molecules, have been shown to be involved in the induction and maintenance of cambium and the formation of secondary vascular tissues. The control of xylem cell patterning is of particular interest, because it determines the diameter of xylem vessels, which is central to the efficiency of water and nutrient transport from roots to leaves through the stem and may strongly influence the growth in height of the tree. Increasing scientific evidence have proved the role of other hormones in cambial cell activities and the study of the hormonal signals and their crosstalking in cambial cells may foster our understanding of the dynamics of xylogenesis and of the mechanism of vessel size control along the stem. In this article, the role of the hormonal signals involved in the control of cambium and xylem development in trees and their crosstalking are reviewed.

Effects of temperature and water deficit on cambial activity and woody ring features in Picea mariana saplings

Increase in temperature under the projected future climate change would affect tree growth, including the physiological mechanisms related to sapling responses, which has been examined recently. The study investigated the plant water relations, cambial activity and wood formation in black spruce saplings [Picea mariana (Mill.) B.S.P.] subjected to water deficit and warming. Four-year-old saplings growing in three greenhouses were submitted to different thermal conditions: T0, with a temperature equal to the external air temperature; and T + 2 and T + 5, with temperatures set at 2 and 5 K higher than T0, respectively. We also submitted saplings to two irrigation regimes and studied the effects of a water deficit of 32 days in May-June. We evaluated plant water relations, cambial activity, wood formation and anatomical characteristics from May to October 2010. Lower needle physiology rates were observed during water deficit, with 20-day suspension of irrigation, but after re-watering, non-irrigated saplings attained the same values as irrigated ones in all thermal conditions. Significant differences between irrigation regimes were detected in cambial activity at the end of the water deficit and after resumption of irrigation. Under warmer conditions, the recovery of non-irrigated saplings was slower than T0 and they needed from 2 to 4 weeks to completely restore cambial activity. No significant differences in wood anatomy were observed between irrigation regimes, but there was a sporadic effect on wood density under warming. During wood formation, the warmer conditions combined with water deficit increased sapling mortality by 5 and 12.2% for T + 2 and T + 5, respectively. The black spruce saplings that survived were more sensitive to water availability, and the restoration of cambial activity was slower at temperatures higher than T0. Our results suggest that black spruce showed a plastic response to intense water deficit under warming, but this would compromise their survival.

How do drought and warming influence survival and wood traits of Picea mariana saplings

Highlight Night and day warming combined with drought affect wood anatomy and survival, reflecting the importance of carbon–water relations for the survival process in Picea mariana saplings.

Compensatory mechanisms mitigate the effect of warming and drought on wood formation

Because of global warming, high-latitude ecosystems are expected to experience increases in temperature and drought events. Wood formation will have to adjust to these new climatic constraints to maintain tree mechanical stability and long-distance water transport. The aim of this study is to understand the dynamic processes involved in wood formation under warming and drought. Xylogenesis, gas exchange, water relations and wood anatomy of black spruce [Picea mariana (Mill.) B.S.P.] saplings were monitored during a greenhouse experiment where temperature was increased during daytime or night-time (+6 °C) combined with a drought period. The kinetics of tracheid development expressed as rate and duration of the xylogenesis sub-processes were quantified using generalized additive models. Drought and warming had a strong influence on cell production, but little effect on wood anatomy. The increase in cell production rate under warmer temperatures, and especially during the night-time warming at the end of the growing season, resulted in wider tree-rings. However, the strong compensation between rates and durations of cell differentiation processes mitigates warming and drought effects on tree-ring structure. Our results allowed quantification of how wood formation kinetics is regulated when water and heat stress increase, allowing trees to adapt to future environmental conditions.

Do tree-ring traits reflect different water deficit responses in young poplar clones (Populus × canadensis Mönch ‘I-214’ and P. deltoides ‘Dvina’)?

Poplar clones are known to display a wide range of tolerance to drought and water-use efficiency, but the effects of water deficit on stem growth and tree-ring characteristics are rarely taken into account. This study was conducted in order to investigate whether the main tree-ring traits correlate with irrigation regimes during the growing season in ‘I-214’ and ‘Dvina’ 4-year-old poplar clone saplings grown in concrete tanks, during three consecutive years. Total carbon, stable carbon isotope, Klason lignin and α-cellulose contents were analyzed to characterize wood biochemistry; ring width, wood density, mean vessel density and mean vessel lumen area were analyzed to characterize wood anatomy to assess the influence of irrigation regime. In both clones, wood formed in 2005 was more enriched in 13C, suggesting drought-induced stomatal closure. Wood formed in 2006 was less variable in δ13C in relation to irrigation regimes. ‘Dvina’ showed higher Klason lignin content and wood density than ‘I-214’, whatever the irrigation regime, despite the larger ring widths. ‘Dvina’ has the potential to recover promptly after drought stress, but at the expense of poor wood technological properties, while ‘I-214’ could continue to grow more uniformly under limited water availability, though at a lower rate.

Xylem morphology determines the drought response of two Arundo donax ecotypes from contrasting habitats

Arundo donax exhibits rapid growth and requires little nutrient input, making it an ideal perennial biomass crop species. However, this growth is accompanied by high rates of water use, potentially restricting the use of A. donax in rain‐fed marginal lands. Here, we investigated the physiological and morphological responses to drought in two ecotypes of A. donax from contrasting habitats: one from an arid environment in Morocco, and the second from a warm humid sub‐Mediterranean climate in central Italy. Prolonged drought resulted in identical reductions in leaf‐level photosynthesis (PN) and stomatal conductance (Gs) in the two ecotypes. However, water deficit induced an increase in xylem vessel diameter in the Moroccan plants, improving the movement of water along the stem, but also likely reducing the resistance to embolism. In contrast, the Italian ecotype reduced xylem vessel area, thus increasing resistance to water transport and xylem embolism. The increased xylem vessel size and associated vulnerability to embolism in the Moroccan plants may have contributed to an increase in the loss of leaf numbers, but also to higher relative water content (RWC) in the remaining leaves in comparison to the Italian ecotype, where a greater number of leaves persisted. Despite the Moroccan plants possessing stems with a lower basal area than their Italian counterparts, both ecotypes exhibited identical leaf to supporting stem area ratios under both control and water deficit conditions. This may account for the similarities observed in leaf area measures of PN and Gs in this and previous studies of different A. donax ecotypes. Selection of A. donax ecotypes on the basis of xylem responses to drought may facilitate the development of varieties suited to arid environments prone to severe drought and wetter habitats where prolonged droughts occur less frequently.

Transcript Accumulation Dynamics of Phenylpropanoid Pathway Genes in the Maturing Xylem and Phloem of Picea abies during Latewood Formation

In temperate regions, latewood is produced when cambial activity declines with the approach of autumnal dormancy. The understanding of the temporal (cambium activity vs dormancy) and spatial (phloem, cambial region, maturing xylem) regulation of key genes involved in the phenylpropanoid pathway during latewood formation represents a crucial step towards providing new insights into the molecular basis of xylogenesis. In this study, the temporal pattern of transcript accumulation of 12 phenylpropanoid genes (PAL1, C4H3/5, C4H4, 4CL3, 4CL4, HCT1, C3H3, CCoAOMT1, COMT2, COMT5, CCR2) was analyzed in maturing xylem and phloem of Picea abies during latewood formation. Quantitative reverse transcription-polymerase chain reaction analyses revealed a well-defined RNA accumulation pattern of genes involved in the phenylpropanoid pathway during latewood formation. Differences in the RNA accumulation patterns were detected between the different tissue types analyzed. The results obtained here demonstrated that the molecular processes involved in monolignol biosynthesis are not restricted to the cambial activity timeframe but continued after the end of cambium cell proliferation. Furthermore, since it has been shown that lignification of maturing xylem takes place in late autumn, we argue on the basis of our data that phloem could play a key role in the monolignol biosynthesis process.