SUMMARY
Drought is a major limitation for survival and growth in plants. With more frequent and severe drought episodes occurring due to climate change, it is imperative to understand the genomic and ...physiological basis of drought tolerance to be able to predict how species will respond in the future. In this study, univariate and multitrait multivariate genome‐wide association study methods were used to identify candidate genes in two iconic and ecosystem‐dominating species of the western USA, coast redwood and giant sequoia, using 10 drought‐related physiological and anatomical traits and genome‐wide sequence‐capture single nucleotide polymorphisms. Population‐level phenotypic variation was found in carbon isotope discrimination, osmotic pressure at full turgor, xylem hydraulic diameter, and total area of transporting fibers in both species. Our study identified new 78 new marker × trait associations in coast redwood and six in giant sequoia, with genes involved in a range of metabolic, stress, and signaling pathways, among other functions. This study contributes to a better understanding of the genomic basis of drought tolerance in long‐generation conifers and helps guide current and future conservation efforts in the species.
Significance Statement
Climate change brings more frequent and severe drought events that challenge the survival of natural populations of plants. While most of our knowledge about drought tolerance comes from annual and domesticated plants, the genomic basis of drought tolerance in long‐generation trees is poorly understood. Here, we aim to fill this gap by identifying candidate genes in two conifer species, coast redwood and giant sequoia.
We compared the physiology and growth of seedlings originating from different Sequoia sempervirens (D. Don.) Endl. (coast redwood) and Sequoiadendron giganteum (Lindl.) Buchh. (giant sequoia) ...populations subjected to progressive drought followed by a recovery period in a controlled greenhouse experiment. Our objective was to examine how multiple plant traits interact to influence the response of seedlings of each species and seed population to a single drought and recovery cycle. We measured soil and plant water status, leaf gas exchange, stem embolism and growth of control (well-watered) and drought-stressed (water withheld) seedlings from each population at the beginning, middle and end of a 6-week drought period and again 2 weeks after re-watering. The drought had a significant effect on many aspects of seedling performance, but water-stressed seedlings regained most physiological functioning by the end of the recovery period. Sequoiadendron seedlings exhibited a greater degree of isohydry (water status regulation), lower levels of stem embolism, higher biomass allocation to roots and lower sensitivity of growth to drought compared with Sequoia. Only minor intra-specific differences were observed among populations. Our results show that seedlings of the two redwood species exhibit contrasting drought-response strategies that align with the environmental conditions these trees experience in their native habitats, and demonstrate trade-offs and coordination among traits affecting plant water use, carbon gain and growth under drought.
Abstract
The giant sequoia (Sequoiadendron giganteum) of California are massive, long-lived trees that grow along the U.S. Sierra Nevada mountains. Genomic data are limited in giant sequoia and ...producing a reference genome sequence has been an important goal to allow marker development for restoration and management. Using deep-coverage Illumina and Oxford Nanopore sequencing, combined with Dovetail chromosome conformation capture libraries, the genome was assembled into eleven chromosome-scale scaffolds containing 8.125 Gbp of sequence. Iso-Seq transcripts, assembled from three distinct tissues, was used as evidence to annotate a total of 41,632 protein-coding genes. The genome was found to contain, distributed unevenly across all 11 chromosomes and in 63 orthogroups, over 900 complete or partial predicted NLR genes, of which 375 are supported by annotation derived from protein evidence and gene modeling. This giant sequoia reference genome sequence represents the first genome sequenced in the Cupressaceae family, and lays a foundation for using genomic tools to aid in giant sequoia conservation and management.
As the only species exceeding 90 m in height and 2000 years of age,
Sequoia sempervirens
and
Sequoiadendron giganteum
provide the optimal platform upon which to examine interactions among tree ...structure, age, and growth. We climbed 140 trees in old-growth redwood forests across California, USA, spanning a broad range of sizes and including the tallest, largest, and oldest known living individuals (i.e., 115.86 vs. 96.29 m tall, 424 vs. 582 Mg aboveground dry mass, and 2510 vs. 3240 years old for
Sequoia
and
Sequoiadendron
, respectively). We used a combination of direct measurements, hierarchical sampling, and dendrochronology to quantify tree structure and annual growth increments through old age. We also developed equations to predict aboveground attributes of standing redwoods via ground-based measurements. Compared to
Sequoia
,
Sequoiadendron
develops thicker bark on lower trunks, provisions leaves with more sapwood, and delays heartwood production throughout the crown. Main trunk wood volume growth (up to 1.6 vs. 0.9 m
3
/yr), aboveground biomass growth (up to 0.77 vs. 0.45 Mg/yr), and aboveground growth efficiency (0.55 ± 0.04 vs. 0.22 ± 0.01 kg annual growth per kg leaves, mean ± SE) are all higher in
Sequoia
. Two independent dimensions of structure-size and aboveground vigor-are the strongest predictors of tree-level productivity in both species. A third dimension, relative trunk size, is a significant predictor of growth in
Sequoia
such that trees with relatively large main trunks compared to their crowns produce more wood annually. Similar-size trees grow at similar rates regardless of latitude or elevation in tall forests of each species. Recent annual growth increments are higher than in the past for the majority of trees, and old trees are just as responsive to environmental changes as young trees. Negative growth-age relationships in previous centuries and positive growth-age relationships in recent decades reflect sampling bias and shifting disturbance regimes. Overall, we find little (if any) evidence for negative effects of old age on tree-level productivity in either species. Except for recovery periods following temporary reductions in crown size, annual increments of wood volume and biomass growth increase as redwoods enlarge with age until extrinsic forces cause tree death.
PREMISE OF THE STUDY: Leaves respond to environmental signals and acclimate to local conditions until their ecological limits are reached. Understanding foliar response to climate change, as it ...expands our knowledge of tree physiology. METHODS: We examined foliar anatomy and morphology of the largest plant species, Sequoiadendron giganteum, from leafy shoot samples collected throughout crowns of trees up to 95 m tall and assessed the functionality of within-crown variation with a novel drought/recovery experiment. KEY RESULTS: We found phenotypic variation in response to water availability in 13 anatomical traits of Sequoiadendron leaves. Shoot expansion was constrained by the hydrostatic gradient of maximum water potential, while functional traits supporting succulence and toughness were associated with sites of peak hydraulic limitation. Water-stress tolerance in experimental shoots increased dramatically with height. CONCLUSION: We propose a heat-sink function for transfusion tissue and uncover a suite of traits suggesting rapid hydraulic throughput and flexibility in water-stress tolerance investments as strategies that help this montane species reach such enormous size. Responses to water stress alter the amount of carbon stored in foliage and the rate of the eventual release of carbon.
The influences of (1) a high fiber content, (2) the arrangement of fibers in fiber groups, and (3) a layered hierarchical composition of the bark of the giant sequoia (
) on its energy dissipation ...capability are analyzed and discussed regarding the relevance for an application in bioinspired components in civil engineering. The giant sequoia is native to the Sierra Nevada (USA), a region with regular rockfalls. It is thus regularly exposed to high-energy impacts, with its bark playing a major protective role, as can be seen in the wild and has been proven in laboratory experiments. The authors quantify the fundamental biomechanical properties of the bark at various length scales, taking into account its hierarchical setup ranging from the integral level (whole bark) down to single bark fibers. Microtensile tests on single fibers and fiber pairs give insights into the properties of single fibers as well as the benefits of the strong longitudinal interconnection between single fibers arranged in pairs. Going beyond the level of single fibers or fiber pairs, towards the integral level, quasistatic compression tests and dynamic impact tests are performed on samples comprising the whole bark (inner and outer bark). These tests elucidate the deformation behavior under quasistatic compression and dynamic impact relevant for the high energy dissipation and impact-damping behavior of the bark. The remarkable energy dissipation capability of the bark at the abovementioned hierarchical levels are linked to the layered and fibrous structure of the bark structurally analyzed by thin sections and SEM and µCT scans.
Dissecting the genomic basis of local adaptation is a major goal in evolutionary biology and conservation science. Rapid changes in the climate pose significant challenges to the survival of natural ...populations, and the genomic basis of long-generation plant species is still poorly understood. Here, we investigated genome-wide climate adaptation in giant sequoia and coast redwood, two iconic and ecologically important tree species. We used a combination of univariate and multivariate genotype-environment association methods and a selective sweep analysis using non-overlapping sliding windows. We identified genomic regions of potential adaptive importance, showing strong associations to moisture variables and mean annual temperature. Our results found a complex architecture of climate adaptation in the species, with genomic regions showing signatures of selective sweeps, polygenic adaptation, or a combination of both, suggesting recent or ongoing climate adaptation along moisture and temperature gradients in giant sequoia and coast redwood. The results of this study provide a first step toward identifying genomic regions of adaptive significance in the species and will provide information to guide management and conservation strategies that seek to maximize adaptive potential in the face of climate change.
Premise
Patterns of genetic structure across a species’ range reflect the long‐term interplay between genetic drift, gene flow, and selection. Given the importance of gene flow in preventing the loss ...of diversity through genetic drift among spatially isolated populations, understanding the dynamics of gene flow and the factors that influence connectivity across a species’ range is a major goal for conservation of genetic diversity. Here we present a detailed look at gene flow dynamics of Sequoiadendron giganteum, a paleoendemic tree species that will likely face numerous threats due to climate change.
Methods
We used microsatellite markers to examine nineteen populations of S. giganteum for patterns of genetic structure and to estimate admixture and rates of gene flow between eight population pairs. Also, we used Generalized Dissimilarity Models to elucidate landscape factors that shape genetic differentiation among populations.
Results
We found minimal gene flow between adjacent groves in the northern disjunct range. In most of the southern portion of the range, groves showed a signal of connectivity which degrades to isolation in the extreme south. Geographic distance was the most important predictor of genetic dissimilarity across the range, with environmental conditions related to precipitation and temperature explaining a small, but significant, portion of the genetic variance.
Conclusions
Due to their isolation and unique genetic composition, northern populations of S. giganteum should be considered a high conservation priority. In this region, we suggest germplasm conservation as well as restoration planting to enhance genetic diversity.
Abstract Key message Dendroclimatic sensitivity varies by axial position for Sequoiadendron giganteum : negative correlations with June temperature strengthen with height, while positive correlations ...with snow water are strongest in the lower trunk. Increment cores collected along trunks of mature Sequoiadendron giganteum provide new and updated ring-width chronologies ideal for assessing how height above ground affects sensitivity of radial growth to climatic variation. Chronologies from 61 living trees at nine locations across the geographic distribution span 1973 yr. Analyses of subsets of 18–44 trees reveal that correlations between radial increments and climate (temperature, water availability) vary with axial position. Negative correlations with maximum and minimum June temperature intensify with height and are strongest at the highest position analyzed (60 m above ground). Sensitivity to the hydroclimate variable of April-1 snow water equivalent is stronger at lower trunk positions (10 m) compared to breast height or the upper trunk, and a similar relationship is identified for the standardized precipitation evapotranspiration index using a 12-month window ending in September. Drought-induced low-growth years computed as radial increment relative to the mean of 10 yr before and after are more weakly expressed at breast height compared to higher on the trunk (10–60 m). Analysis of regional upper (maximum core height = 87 m) versus lower trunk (above buttress) chronologies corroborate differing inter-annual correlations with climate depending on height above ground. Accounting for axial variation in dendroclimatic sensitivity can maximize the quality of environmental reconstructions using tree rings and improve biophysical understanding of Sequoiadendron , especially in the context of an increasingly arid climate.
•Giant sequoias showed unprecedented foliage dieback during recent, extreme drought.•The magnitude of foliage dieback was highly variable within and among sequoia groves.•Foliage dieback was ...correlated with metrics related to site water balance.•Results contribute to our broader understanding of sequoia drought vulnerability.
Hotter droughts – droughts in which unusually high temperatures exacerbate the effects of low precipitation – are expected to increase in frequency and severity in coming decades, challenging scientists and managers to identify which parts of forested landscapes may be most vulnerable. In 2014, in the middle of California’s historically unprecedented 2012–2016 hotter drought, we noticed apparently drought-induced foliage dieback in giant sequoias (Sequoiadendron giganteum Lindl. Buchholz) in Sequoia and Kings Canyon national parks, California. Characteristics of the dieback were consistent with a controlled process of drought-induced senescence: younger (distal) shoots remained green while older (proximal) shoots were preferentially shed. As part of an ongoing interdisciplinary effort to understand and map sequoia vulnerability to hotter droughts, we reviewed historical records for evidence of previous foliage dieback events, surveyed dieback along trail corridors in eight sequoia groves, and analyzed tree-ring data from a high- and a low-foliage-dieback area. In sharp contrast to the greatly elevated mortality of other coniferous species found at low and middle elevations, we estimate that <1% of sequoias died during the drought. Foliage dieback was notably elevated in 2014 – the most severe single drought year in our 122-year record – but much lower in subsequent years. We found no historical records of similar foliage dieback during previous droughts. Dieback in 2014 was highly variable both within and among groves, ranging from virtually no dieback in some areas to nearly 50% in others. Dieback was highest (1) at low elevations, probably due to higher temperatures, reduced snowpack, and earlier snowmelt; (2) in areas of low adult sequoia densities, which likely reflect intrinsically more stressful sites; and (3) on steep slopes, probably reflecting reduced water availability. Average sequoia ring widths were narrower at the high-dieback than the low-dieback tree-ring site, but for reasons that remain unclear the sites did not differ in their proportional ring-width responses to past droughts. Collectively, our results suggest that giant sequoia vulnerability to hotter droughts may be spatially quite variable, and that at least some of that variability can be explained by metrics related to site water balance. Future research will focus on integrating our results with physiological and remote-sensing data, including tracking sequoias as they recover from the drought.
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