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25 May 2024, Volume 46 Issue 03
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  • Articles
    Evolutionary history shapes variation of wood density of tree species across the world
    Fangbing Li, Hong Qian, Jordi Sardans, Dzhamal Y. Amishev, Zixuan Wang, Changyue Zhang, Tonggui Wu, Xiaoniu Xu, Xiao Tao, Xingzhao Huang
    2024, 46(03):  283-293.  doi:10.1016/j.pld.2024.04.002
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    The effect of evolutionary history on wood density variation may play an important role in shaping variation in wood density, but this has largely not been tested. Using a comprehensive global dataset including 27,297 measurements of wood density from 2621 tree species worldwide, we test the hypothesis that the legacy of evolutionary history plays an important role in driving the variation of wood density among tree species. We assessed phylogenetic signal in different taxonomic (e.g., angiosperms and gymnosperms) and ecological (e.g., tropical, temperate, and boreal) groups of tree species, explored the biogeographical and phylogenetic patterns of wood density, and quantified the relative importance of current environmental factors (e.g., climatic and soil variables) and evolutionary history (i.e., phylogenetic relatedness among species and lineages) in driving global wood density variation. We found that wood density displayed a significant phylogenetic signal. Wood density differed among different biomes and climatic zones, with higher mean values of wood density in relatively drier regions (highest in subtropical desert). Our study revealed that at a global scale, for angiosperms and gymnosperms combined, phylogeny and species (representing the variance explained by taxonomy and not direct explained by long-term evolution process) explained 84.3% and 7.7% of total wood density variation, respectively, whereas current environment explained 2.7% of total wood density variation when phylogeny and species were taken into account. When angiosperms and gymnosperms were considered separately, the three proportions of explained variation are, respectively, 84.2%, 7.5% and 6.7% for angiosperms, and 45.7%, 21.3% and 18.6% for gymnosperms. Our study shows that evolutionary history outpaced current environmental factors in shaping global variation in wood density.
    Conservation genomics provides insights into genetic resilience and adaptation of the endangered Chinese hazelnut, Corylus chinensis
    Zhen Yang, Lisong Liang, Weibo Xiang, Lujun Wang, Qinghua Ma, Zhaoshan Wang
    2024, 46(03):  294-308.  doi:10.1016/j.pld.2024.03.006
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    Global climate change has increased concerns regarding biodiversity loss. However, many key conservation issues still required further research, including demographic history, deleterious mutation load, adaptive evolution, and putative introgression. Here we generated the first chromosome-level genome of the endangered Chinese hazelnut, Corylus chinensis, and compared the genomic signatures with its sympatric widespread C. kwechowensis-C. yunnanensis complex. We found large genome rearrangements across all Corylus species and identified species-specific expanded gene families that may be involved in adaptation. Population genomics revealed that both C. chinensis and the C. kwechowensis-C. yunnanensis complex had diverged into two genetic lineages, forming a consistent pattern of southwestern-northern differentiation. Population size of the narrow southwestern lineages of both species have decreased continuously since the late Miocene, whereas the widespread northern lineages have remained stable (C. chinensis) or have even recovered from population bottlenecks (C. kwechowensis-C. yunnanensis complex) during the Quaternary. Compared with C. kwechowensis-C. yunnanensis complex, C. chinensis showed significantly lower genomic diversity and higher inbreeding level. However, C. chinensis carried significantly fewer deleterious mutations than C. kwechowensis-C. yunnanensis complex, as more effective purging selection reduced the accumulation of homozygous variants. We also detected signals of positive selection and adaptive introgression in different lineages, which facilitated the accumulation of favorable variants and formation of local adaptation. Hence, both types of selection and exogenous introgression could have mitigated inbreeding and facilitated survival and persistence of C. chinensis. Overall, our study provides critical insights into lineage differentiation, local adaptation, and the potential for future recovery of endangered trees.
    Multi-omics analyses provide insights into the evolutionary history and the synthesis of medicinal components of the Chinese wingnut
    Zi-Yan Zhang, He-Xiao Xia, Meng-Jie Yuan, Feng Gao, Wen-Hua Bao, Lan Jin, Min Li, Yong Li
    2024, 46(03):  309-320.  doi:10.1016/j.pld.2024.03.010
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    Chinese wingnut (Pterocarya stenoptera) is a medicinally and economically important tree species within the family Juglandaceae. However, the lack of high-quality reference genome has hindered its in-depth research. In this study, we successfully assembled its chromosome-level genome and performed multi-omics analyses to address its evolutionary history and synthesis of medicinal components. A thorough examination of genomes has uncovered a significant expansion in the Lateral Organ Boundaries Domain gene family among the winged group in Juglandaceae. This notable increase may be attributed to their frequent exposure to flood-prone environments. After further differentiation between Chinese wingnut and Cyclocarya paliurus, significant positive selection occurred on the genes of NADH dehydrogenase related to mitochondrial aerobic respiration in Chinese wingnut, enhancing its ability to cope with waterlogging stress. Comparative genomic analysis revealed Chinese wingnut evolved more unique genes related to arginine synthesis, potentially endowing it with a higher capacity to purify nutrient-rich water bodies. Expansion of terpene synthase families enables the production of increased quantities of terpenoid volatiles, potentially serving as an evolved defense mechanism against herbivorous insects. Through combined transcriptomic and metabolomic analysis, we identified the candidate genes involved in the synthesis of terpenoid volatiles. Our study offers essential genetic resources for Chinese wingnut, unveiling its evolutionary history and identifying key genes linked to the production of terpenoid volatiles.
    Across two phylogeographic breaks: Quaternary evolutionary history of a mountain aspen (Populus rotundifolia) in the Hengduan Mountains
    Jieshi Tang, Xiaoyan Fan, Richard I. Milne, Heng Yang, Wenjing Tao, Xinran Zhang, Mengyun Guo, Jialiang Li, Kangshan Mao
    2024, 46(03):  321-332.  doi:10.1016/j.pld.2024.03.009
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    Biogeographical barriers to gene flow are central to plant phylogeography. In East Asia, plant distribution is greatly influenced by two phylogeographic breaks, the Mekong-Salween Divide and Tanaka-Kaiyong Line, however, few studies have investigated how these barriers affect the genetic diversity of species that are distributed across both. Here we used 14 microsatellite loci and four chloroplast DNA fragments to examine genetic diversity and distribution patterns of 49 populations of Populus rotundifolia, a species that spans both the Mekong-Salween Divide and the Tanaka-Kaiyong Line in southwestern China. Demographic and migration hypotheses were tested using coalescent-based approaches. Limited historical gene flow was observed between the western and eastern groups of P. rotundifolia, but substantial flow occurred across both the Mekong-Salween Divide and Tanaka-Kaiyong Line, manifesting in clear admixture and high genetic diversity in the central group. Wind-borne pollen and seeds may have facilitated the dispersal of P. rotundifolia following prevalent northwest winds in the spring. We also found that the Hengduan Mountains, where multiple genetic barriers were detected, acted on the whole as a barrier between the western and eastern groups of P. rotundifolia. Ecological niche modeling suggested that P. rotundifolia has undergone range expansion since the last glacial maximum, and demographic reconstruction indicated an earlier population expansion around 600 Ka. The phylogeographic pattern of P. rotundifolia reflects the interplay of biological traits, wind patterns, barriers, niche differentiation, and Quaternary climate history. This study emphasizes the need for multiple lines of evidence in understanding the Quaternary evolution of plants in topographically complex areas.
    Central Asia revealed as a key area in evolution of Eremurus (Asphodelaceae)
    Dilmurod Makhmudjanov, Sergei Volis, Ziyoviddin Yusupov, Inom Juramurodov, Komiljon Tojibaev, Tao Deng, Hang Sun
    2024, 46(03):  333-343.  doi:10.1016/j.pld.2023.08.004
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    Eremurus was described at the beginning of the 19th century. However, due to limited sampling and the small number of gene markers to date, its phylogeny and evolution are largely unknown. In this study, we analyzed plastomes from 27 species belonging to 2 subgenera and 3 sections of Eremurus, which are found in Central Asia (its center of diversity) and China. We also analyzed nuclear DNA ITS of 33 species, encompassing all subgenera and sections of the genus in Central Asia, southwest Asia and China. Our findings revealed that the genus was monophyletic, although both subgenera Eremurus and Henningia were found to be paraphyletic. Both plastome and nrDNA-based phylogenetic trees had three clades that did not reflect the current taxonomy of the genus. Our biogeographical and time-calibrated trees suggest that Eremurus originated in the ancient Tethyan area in the second half of the Eocene. Diversification of Eremurus occurred from the early Oligocene to the late Miocene. Paratethys Sea retreat and several orogenetic events, such as the progressive uplift of the Qinghai-Tibet Plateau and surrounding mountain belts (Altai, Pamir, Tian Shan), caused serious topographic and climate (aridification) changes in Central Asia that may have triggered a split of clades and speciation. In this transformed Central Asia, speciation proceeded rapidly driven mainly by vicariance caused by numerous mountain chains and specialization to a variety of climatic, topographic and soil conditions that exist in this region.
    Deep genome skimming reveals the hybrid origin of Pseudosasa gracilis (Poaceae: Bambusoideae)
    Xiang-Zhou Hu, Cen Guo, Sheng-Yuan Qin, De-Zhu Li, Zhen-Hua Guo
    2024, 46(03):  344-352.  doi:10.1016/j.pld.2023.06.001
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    Pseudosasa gracilis (Poaceae:Bambusoideae) is a temperate woody bamboo species endemic to South-central China with a narrow distribution. Previous phylogenetic studies revealed an unexpected, isolated phylogenetic position of Ps. gracilis. Here we conducted phylogenomic analysis by sampling populations of Ps. gracilis and its sympatric species Ps. nanunica and Sinosasa polytricha reflecting different genomic signals, by deep genome skimming. Integrating molecular evidence from chloroplast genes and genome-wide SNPs, we deciphered the phylogenetic relationships of Ps. gracilis. Both plastid and nuclear data indicate that Ps. gracilis is more closely related to Sinosasa, which is discordant with the taxonomic treatment. To further explore this molecular-morphological conflict, we screened 411 "perfect-copy" syntenic genes to reconstruct phylogenies using both the concatenation and coalescent methods. We observed extensive discordance between gene trees and the putative species tree. A significant hybridization event was detected based on 411 genes from the D subgenome, showing Ps. gracilis was a hybrid descendant between Sinosasa longiligulata and Ps. nanunica, with 63.56% and 36.44% inheritance probabilities of each parent. Moreover, introgression events were detected in the C subgenome between Ps. gracilis and S. polytricha in the same distribution region. Our findings suggest that sympatric hybridization and introgression play a crucial role in the origin of Ps. gracilis. By providing an empirical example of bamboo of hybrid origin using comprehensive analyses based on genomic data from different inheritance systems and morphological characters, our study represents a step forward in understanding of reticulate evolution of bamboos.
    Species' geographical range, environmental range and traits lead to specimen collection preference of dominant plant species of grasslands in Northern China
    Jingya Zhang, Cui Xiao, Xiaoyu Duan, Xin Gao, Hao Zeng, Rong'an Dong, Gang Feng, Keping Ma
    2024, 46(03):  353-361.  doi:10.1016/j.pld.2024.02.001
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    Many different factors, such as species traits, socio-economic factors, geographical and environmental factors, can lead to specimen collection preference. This study aims to determine whether grassland specimen collection in China is preferred by species traits (i.e., plant height, flowering and fruiting period), environmental range (i.e., the temperature and precipitation range) and geographical range (i.e., distribution range and altitudinal range). Ordinary least squares models and phylogenetic generalized linear mixed models were used to analyze the relationships between specimen number and the explanatory variables. Random Forest models were then used to find the most parsimonious multivariate model. The results showed that interannual variation in specimen number between 1900 and 2020 was considerable. Specimen number of these species in southeast China was notably lower than that in northwest China. Environmental range and geographical range of species had significant positive correlations with specimen number. In addition, there were relatively weak but significant associations between specimen number and species trait (i.e., plant height and flowering and fruiting period). Random Forest models indicated that distribution range was the most important variable, followed by flowering and fruiting period, and altitudinal range. These findings suggest that future floristic surveys should pay more attention to species with small geographical range, narrow environmental range, short plant height, and short flowering and fruiting period. The correction of specimen collection preference will also make the results of species distribution model, species evolution and other works based on specimen data more accurate.
    Arlenea delicata gen. et sp. nov., a new ephedroid plant from the Early Cretaceous Crato Formation, Araripe Basin, Northeast Brazil
    Alita Maria Neves Ribeiro, Yong Yang, Antônio Álamo Feitosa Saraiva, Renan Alfredo Machado Bantim, João Tavares Calixto Junior, Flaviana Jorge de Lima
    2024, 46(03):  362-371.  doi:10.1016/j.pld.2023.06.008
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    Ephedroid macrofossils have been widely documented in Cretaceous deposits, including numerous from the Lower Cretaceous Yixian Formation of NE China. However, few ephedroid macrofossils have been reported from South America. Herein, we describe a new plant of the family Ephedraceae, Arlenea delicata gen. et sp. nov., from the Lower Cretaceous Crato Formation of the Araripe Basin, Northeast Brazil, based on the vegetative and reproductive structures. It has the typical morphological characteristics of ephedroid plants, including fertile reproductive branches, opposite phyllotaxy, terminal female cones, a sympodial branching system, longitudinally striated internodes, and swollen nodes. Our new finding is unusual in having inner chlamydosperms subtended by two pairs of bracts, reproductive units connected to branches through swollen receptacles and a smooth seed surface. This new ephedroid taxon from the Crato Formation increases our understanding of plant diversity of this group during the Early Cretaceous. Furthermore, the general morphology (fleshy bracts and enlarged receptacles) of this new fossil discovery indicates that seeds of this plant may have been dispersed by animals such as pterosaurs (mainly the Tapejaridae) and birds (Enantiornithes and Ornituromorpha). If true, this would explain the cosmopolitan distribution of Ephedraceae in the Lower Cretaceous.
    Comprehensive integration of single-cell transcriptomic data illuminates the regulatory network architecture of plant cell fate specification
    Shanni Cao, Xue Zhao, Zhuojin Li, Ranran Yu, Yuqi Li, Xinkai Zhou, Wenhao Yan, Dijun Chen, Chao He
    2024, 46(03):  372-385.  doi:10.1016/j.pld.2024.03.008
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    Plant morphogenesis relies on precise gene expression programs at the proper time and position which is orchestrated by transcription factors (TFs) in intricate regulatory networks in a cell-type specific manner. Here we introduced a comprehensive single-cell transcriptomic atlas of Arabidopsis seedlings. This atlas is the result of meticulous integration of 63 previously published scRNA-seq datasets, addressing batch effects and conserving biological variance. This integration spans a broad spectrum of tissues, including both below- and above-ground parts. Utilizing a rigorous approach for cell type annotation, we identified 47 distinct cell types or states, largely expanding our current view of plant cell compositions. We systematically constructed cell-type specific gene regulatory networks and uncovered key regulators that act in a coordinated manner to control cell-type specific gene expression. Taken together, our study not only offers extensive plant cell atlas exploration that serves as a valuable resource, but also provides molecular insights into gene-regulatory programs that varies from different cell types.
    Epigenetic control on transcription of vernalization genes and whole-genome gene expression profile induced by vernalization in common wheat
    Yunzhen Li, Liujie Jin, Xinyu Liu, Chao He, Siteng Bi, Sulaiman Saeed, Wenhao Yan
    2024, 46(03):  386-394.  doi:10.1016/j.pld.2024.02.005
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    Vernalization is necessary for winter wheat to flower. However, it is unclear whether vernalization is also required for spring wheat, which is frequently sown in fall, and what molecular mechanisms underlie the vernalization response in wheat varieties. In this study, we examined the molecular mechanisms that regulate vernalization response in winter and spring wheat varieties. For this purpose, we determined how major vernalization genes (VRN1, VRN2, and VRN3) respond to vernalization in these varieties and whether modifications to histones play a role in changes in gene expression. We also identified genes that are differentially regulated in response to vernalization in winter and spring wheat varieties. We found that in winter wheat, but not in spring wheat, VRN1 expression decreases when returned to warm temperature following vernalization. This finding may be associated with differences between spring and winter wheat in the levels of tri-methylation of lysine 27 on histone H3 (H3K27me3) and tri-methylation of lysine 4 on histone H3 (H3K4me3) at the VRN1 gene. Analysis of winter wheat transcriptomes before and after vernalization revealed that vernalization influences the expression of several genes, including those involved in leucine catabolism, cysteine biosynthesis, and flavonoid biosynthesis. These findings provide new candidates for further study on the mechanism of vernalization regulation in wheat.
    Stomatal dynamics are regulated by leaf hydraulic traits and guard cell anatomy in nine true mangrove species
    Ya-Dong Qie, Qi-Wei Zhang, Scott A. M. McAdam, Kun-Fang Cao
    2024, 46(03):  395-405.  doi:10.1016/j.pld.2024.02.003
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    Stomatal regulation is critical for mangroves to survive in the hyper-saline intertidal zone where water stress is severe and water availability is highly fluctuant. However, very little is known about the stomatal sensitivity to vapour pressure deficit (VPD) in mangroves, and its co-ordination with stomatal morphology and leaf hydraulic traits. We measured the stomatal response to a step increase in VPD in situ, stomatal anatomy, leaf hydraulic vulnerability and pressure-volume traits in nine true mangrove species of five families and collected the data of genome size. We aimed to answer two questions:(1) Does stomatal morphology influence stomatal dynamics in response to a high VPD in mangroves? with a consideration of possible influence of genome size on stomatal morphology; and (2) do leaf hydraulic traits influence stomatal sensitivity to VPD in mangroves? We found that the stomata of mangrove plants were highly sensitive to a step rise in VPD and the stomatal responses were directly affected by stomatal anatomy and hydraulic traits. Smaller, denser stomata was correlated with faster stomatal closure at high VPD across the species of Rhizophoraceae, and stomata size negatively and vein density positively correlated with genome size. Less negative leaf osmotic pressure at the full turgor (πo) was related to higher operating steady-state stomatal conductance (gs); and a higher leaf capacitance (Cleaf) and more embolism resistant leaf xylem were associated with slower stomatal responses to an increase in VPD. In addition, stomatal responsiveness to VPD was indirectly affected by leaf morphological traits, which were affected by site salinity and consequently leaf water status. Our results demonstrate that mangroves display a unique relationship between genome size, stomatal size and vein packing, and that stomatal responsiveness to VPD is regulated by leaf hydraulic traits and stomatal morphology. Our work provides a quantitative framework to better understand of stomatal regulation in mangroves in an environment with high salinity and dynamic water availability.
    Hydraulic properties and drought response of a tropical bamboo (Cephalostachyum pergracile)
    Wanwalee Kongjarat, Lu Han, Amy Ny Aina Aritsara, Shu-Bin Zhang, Gao-Juan Zhao, Yong-Jiang Zhang, Phisamai Maenpuen, Ying-Mei Li, Yi-Ke Zou, Ming-Yi Li, Xue-Nan Li, Lian-Bin Tao, Ya-Jun Chen
    2024, 46(03):  406-415.  doi:10.1016/j.pld.2023.12.003
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    Bamboo plants are an essential component of tropical ecosystems, yet their vulnerability to climate extremes, such as drought, is poorly understood due to limited knowledge of their hydraulic properties. Cephalostachyum pergracile, a commonly used tropical bamboo species, exhibited a substantially higher mortality rate than other co-occurring bamboos during a severe drought event in 2019, but the underlying mechanisms remain unclear. This study investigated the leaf and stem hydraulic traits related to drought responses, including leaf-stem embolism resistance (P50leaf; P50stem) estimated using optical and X-ray microtomography methods, leaf pressure-volume and water-releasing curves. Additionally, we investigated the seasonal water potentials, native embolism level (PLC) and xylem water source using stable isotope. We found that C. pergracile exhibited strong resistance to embolism, showing low P50leaf., P50stem, and turgor loss point, despite its rapid leaf water loss. Interestingly, its leaves displayed greater resistance to embolism than its stem, suggesting a lack of effective hydraulic vulnerability segmentation (HVS) to protect the stem from excessive xylem tension. During the dry season, approximately 49% of the water was absorbed from the upper 20-cm-deep soil layer. Consequently, significant diurnal variation in leaf water potentials and an increase in midday PLC from 5.87±2.33% in the wet season to 12.87±4.09% in the dry season were observed. In summary, this study demonstrated that the rapid leaf water loss, high reliance on surface water, and a lack of effective HVS in C. pergracile accelerated water depletion and increased xylem embolism even in the typical dry season, which may explain its high mortality rate during extreme drought events in 2019.
    Short communication
    BrrTCP4b interacts with BrrTTG1 to suppress the development of trichomes in Brassica rapa var. rapa
    Cheng Li, Li Zhang, Hefan Li, Yuanwen Duan, Xuemei Wen, Yongping Yang, Xudong Sun
    2024, 46(03):  416-420.  doi:10.1016/j.pld.2024.03.003
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    The number of trichomes significantly increased in CRISPR/Cas9-edited BrrTCP4b turnip (Brassica rapa var. rapa) plants. However, the underlying molecular mechanism remains to be uncovered. In this study, we performed the Y2H screen using BrrTCP4b as the bait, which unveiled an interaction between BrrTCP4b and BrrTTG1, a pivotal WD40-repeat protein transcription factor in the MYB-bHLH-WD40 (MBW) complex. This physical interaction was further validated through bimolecular luciferase complementation and co-immunoprecipitation. Furthermore, it was found that the interaction between BrrTCP4b and BrrTTG1 could inhibit the activity of MBW complex, resulting in decreased expression of BrrGL2, a positive regulator of trichomes development. In contrast, AtTCP4 is known to regulate trichomes development by interacting with AtGL3 in Arabidopsis thaliana. Overall, this study revealed that BrrTCP4b is involved in trichome development by interacting with BrrTTG1 in turnip, indicating a divergence from the mechanisms observed in model plant A. thaliana. The findings contribute to our understanding of the regulatory mechanisms governing trichome development in the non-model plants turnip.
    Molecular analyses display the increasing diversity of Podostemaceae in China
    Zhi-Zhong Li, Zhun Xu, Shuang Wu, Lang-Xing Yuan, Chun-Yu Zou, Yan Liu, Jian-Yong Lin, Shi-Chu Liang
    2024, 46(03):  421-424.  doi:10.1016/j.pld.2024.02.002
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