2020 article

In memory of Professor Tang Yan-Cheng: New perspectives in systematic and evolutionary biology

Xiang, Q.-Y., Chen, Z.-D., Song, B.-H., & Boufford, D. E. (2020, September). JOURNAL OF SYSTEMATICS AND EVOLUTION, Vol. 58, pp. 527–532.

By: Q. Xiang n, Z. Chen*, B. Song* & D. Boufford*

co-author countries: China 🇨🇳 United States of America 🇺🇸
Source: Web Of Science
Added: October 5, 2020

In China, three institutes for botanical research were established in the 1920s, namely the Department of Botany, Biological Laboratory of the Science Society of China (1922, Nanjing), the Fan Memorial Institute of Biology (1928, Peiping), and the Institute of Botany, Peiping Academy of Sciences (1929, Peiping). Since then, plant taxonomy, plant systematics, and phytogeography have advanced and prospered as scientific disciplines in China. Among the great botanists who studied at those institutes, and at others that were established over the following 100 years, was Prof. Tang (surname) Yan-Cheng (given name) (汤彦承, abbreviated Y. C. Tang) (7 July 1926–6 August 2016). Professor Tang was a well-known and highly respected plant taxonomist and an influential professor at the Institute of Botany, Chinese Academy of Sciences, Beijing. Prof. Tang played a pivotal role in leading taxonomic/systematic research in China from the 1970s into the 1990s. He not only provided new insights into the Chinese flora, but also helped to develop Chinese botany according to what were then new cladistic methods and to train the following generations of Chinese botanists. During his career, Prof. Tang keenly promoted novel theories and taxonomic and systematic methods, and he encouraged the application of up-to-date experimental approaches and analytical methodologies to study Chinese plants. His research had global implications for large, widely distributed plant families and provided a better understanding of the origin and evolution of the East Asian flora (see Wang et al., 2020a and more details below). Therefore, in this special issue, we have compiled articles that reflect current advances in plant taxonomy, systematics, and phytogeography to honor the contributions of Prof. Tang. The articles herein, including reviews and original articles, represent new perspectives in systematics and evolution, and also present research that integrates multifaceted data and interdisciplinary approaches. Several articles concern plant taxa studied in depth by Prof. Tang or those that were a focus of his interest. Modern systematic biology originated in the 1960s with the cladistic methods developed and expounded by Hennig (Hennig, 1966; Funk, 2018). In the past 30 years, the discipline of systematic biology has been transformed by the use of molecular approaches and phylogenetics (Hillis et al., 1996; Soltis et al., 1998). Subsequent advancements in molecular technology, phylogenetic methodologies, and comparative methods have led to an explosion of molecular systematics and phylogeny-based comparative studies. The results have led to a better understanding of relationships and evolution of the organisms with which we share our planet (Chase et al., 1993; San Mauro & Agorreta, 2010; Losos et al., 2013; Hinchliff et al., 2015; Soltis & Soltis, 2016; Soltis et al., 2018; Bakker et al., 2020). Moreover, recent efforts in reconstructing the tree of life, integrating methods and sharing data across disciplines, digitizing biological collections, harvesting big data from high-throughput DNA sequencing, and development of analytical and genetic tools (Wen et al., 2015, 2017; Soltis & Soltis, 2016; Soltis et al., 2018; Leebens-Mack et al., 2019; Bakker et al., 2020) have empowered systematic and evolutionary biology to undertake novel and integrative studies from perspectives that were previously impossible (e.g., Chanderbali et al., 2017; Ma et al., 2017a, 2017b; Ellwood et al., 2018; Hodel et al., 2018; Landis et al., 2018; Lewin et al., 2018; Lu et al., 2018; Dong et al., 2019). Plant systematics plays a pivotal role in elucidating the evolution and assembly of the Earth's flora. Among the central applications of systematics is the sustenance, use, and conservation of plant resources, especially under many threats of the Anthropocene, including the modern threat of climate change. How will species adapt to environmental changes and what are the evolutionary constraints and drivers for adaptation? These are central questions in evolutionary ecology and conservation biology. Changing climates and global warming require urgent studies to address these questions through characterizing various factors affecting the rate and capacity of plant adaptability to change. Genetic variability, population structure, and genes/traits selected for local adaptation to environmental biotic and abiotic changes/stresses in a species lay the foundation for its survival. Our knowledge of such traits in regard to forest trees and crop species is particularly important in predicting the sustainability of forests and crops under changing environments and in understanding the constraints and drivers of ecological adaptation. At present, studies that are simultaneously broad in scope and detailed at the levels of plant traits and genes are feasible. By integrating and interfacing cutting-edge tools, we can gain a comprehensive understanding of a species and advance our knowledge regarding plant adaptation to a changing climate. In this special issue, Anderson & Song (2020) present an overview of the recent progress, gaps, and perspectives, as well as integrative approaches regarding the adaptation of plants to climate change. They evaluate the impact of climate change on selection, local adaptation, and species interactions. They also discuss the effects of gene flow and phenotypic plasticity on the way plants respond to climate change. They argue that a comprehensive understanding of eco-evolutionary dynamics will facilitate an understanding of a plant's adaptive potential under a rapid and intense climate change. Additionally, they review the most recent studies using integrating cutting-edge omics and biotechnologies to dissect the genetic basis of plant adaptation to climate change. They conclude that key gaps exist, such as in expanding research foci from model species to a diverse array of non-model natural systems, from identifying candidate genes to validating their functions, from the discovery of causal genes to fitness tests under natural conditions, and from single environmental stress factors to multiple factors that reflect the complex and interactive nature of changing environments. They also highlight the importance of employing cross-disciplinary tools to integrate ecology, evolution, molecular genetics, and systems biology to accurately predict the probability of species to persist in a changing environment. The review of Anderson and Song bridges gaps between subdisciplines and inspires innovative work in the field of plant ecology and evolutionary biology. Modern plant systematics has expanded in scope from characterizing species diversity and relationships to the population level to understanding genetic and genomic variation and population structure at fine scales, as well as to identify the genetic loci associated with local adaptation along spatial and ecological gradients (e.g., climate, soil, and disease). For example, Pais and colleagues present advances made in understanding a non-model tree species, Cornus florida L., by integrating landscape ecology, phylogeography, population genomics, and metabolomics, using genome-wide association studies (GWAS) and traditional community ecology methods (Pais et al., 2017, 2018, 2020). Pais et al. (2017) used this integrative approach and Genotyping By Sequencing (GBS) to identify more than 50 loci under selection for adaptation to local environments (differing in temperature, precipitation, and soil nutrients in the southern Appalachian Mountains, Piedmont Plateau, and coastal plain of North Carolina). In Cornus florida L. (colloquially, “flowering dogwood”), some loci under selection were determined to be associated with dogwood anthracnose disease, which has seriously threatened natural populations. By integrating non-targeted liquid chromatography–mass spectrometry (LC-MS) profiling and GWAS, Pais et al. (2018) discovered that some loci under selection were associated with the production of certain groups of metabolites. One such locus represents an L-type lectin domain containing receptor kinase that is known to be important in providing immunity to disease in plants (Singh & Zimmerli, 2013). In this issue, Pais et al. (2020) report the findings of their studies that cover the whole range of the species in which the locus noted above was again identified as one of the loci under selection. This particular locus, whose function may be validated by genome editing, provides a strong candidate for future studies related to disease resistance. Some of the loci putatively under selection exhibited an abrupt turnover in allele frequencies in populations along the borders of the Hot Continental ecoregion and the range of dogwood anthracnose. Trees harboring alleles adaptive to environmental factors that vary among ecoregions may facilitate future genetic breeding and conservation programs with the goal of developing hardy cultivars of Cornus florida, a popular ornamental species. In this study, Pais and colleagues also evaluated the spatial patterns of genetic variation and population genetic structure and compared the patterns they found for the distribution of dogwood anthracnose. They further explored the relationship between fungal sequences contained in the GBS data of sampled trees and the visual records of disease at sampled locations, and they found that fungal genomic sequences were informative for detecting or predicting disease. Understanding the diversification and adaptation of species remains a challenge for botanists (Losos et al., 2013; Funk, 2018). New insights, however, are increasingly being derived from integrative studies that incorporate phylogenomics, biogeography, ecological modeling, and comparative analyses to elucidate spatiotemporal patterns of evolution and the impact of past climatic change and niche divergence on speciation processes and morphological adaptations (e.g., Blaine Marchant et al., 2016; Visger et al., 2016; Yu et al., 2017; Hearn et al., 2018; Fu et al., 2019; Gao et al., 2019; Kawahara et al., 2019; Martín-Bravo et al., 2019; Du et al., 2020). Two papers in this issue (Lindelof et al., 2020; Zhou et al., 2020) shed new light on the evolutionary history of the eastern Asian–eastern North American (EA–ENA) pattern of geographic disjunction and the post-isolation evolution of disjunct lineages. The EA–ENA biogeographic disjunction has attracted recent attention in the phylogenomic era (e.g., Li et al., 2019; Zhang et al., 2019). Zhou et al. (2020) conducted vigorous phylogenomic and divergence analyses using data generated from microfluid PCR and Fluidigm sequencing. They compared different phylogenetic and dating methods, assessed the conflict between gene trees and species trees, and evaluated the impact of fossil calibrations. They included fossil species in constructing a comprehensively dated phylogeny using the Fossilized Birth Death model as the basis for the biogeographic analysis. They applied a user-defined time slice model for inter-areal dispersal probabilities with the divergence–extinction–cladogenesis (DEC) method to better capture the historical barriers affecting plant migration. By further examining morphological evolution and ecological niches, they sought to understand post-isolation evolution and to identify ecological factors that likely shaped the evolution of sister clades among the EA–ENA disjunctions. This issue also contains a novel integrative study by Lindelof et al. (2020), based on RAD-seq data, on a lineage of Cornus L. (Cornaceae) that bears blue, white, and black fruits. The authors discovered new EA–ENA disjunct clades via phylogenomic analyses. On the basis of a comprehensively dated phylogeny as noted above, the authors reconstructed the biogeographic history and examined the evolutionary divergence between the EA and ENA disjunct pairs. By integrating evidence from the rates and patterns of morphological and molecular evolution, as well as evolutionary shifts in ecological niches, the authors tested the hypothesis of morphostasis between disjunct pairs and greater diversification rates in EA among the EA–ENA disjunct clades (Qian & Ricklefs, 2000; Xiang et al., 2004; Lee et al., 2019). Gaynor et al. (2020) examined the roles of biogeography and ecological niche evolution in shaping species diversification in Diapensiaceae by combing nuclear and plastid gene sequences from gene enrichment derived from newly developed Angiosperm 353 probes. The study demonstrated the phylogenomic utility of the genes and their flanking regions in resolving relationships within families. Abundant molecular data from publicly available databases and increased high-throughput sequencing capacity, coupled with the availability of analytical tools, have enabled considerable advances in spatial phylogenetics. In this field, integration of phylogeny with distributional data was employed to understand spatiotemporal patterns of biodiversity, identify biodiversity hot spots and refugia for conservation, and to uncover evolutionary processes and ecological factors shaping the assembly of contemporary biodiversity in plant communities (e.g., Mishler et al., 2014; Chen et al., 2016, 2018; Pollock et al., 2017; Lu et al., 2018; Miller et al., 2018; Ye et al., 2019). Spatial phylogenetic approaches are particularly powerful at regional scales using regional trees of life. In this issue, Hu et al. (2020) present a study updating the tree of life of the vascular plants of China to the species level, using the genus-level tree from a previous study as the framework (Chen et al., 2016). On the updated phylogeny, Hu et al. (2020) evaluated the taxonomic systems of Chinese vascular plants and listed the non-monophyletic genera that require further investigation. They further explored phylogenetic diversity hot spots at both the genus and species levels and compared the results with previous studies. This large, regional-scale phylogeny will serve as an important basis for future spatial phylogenetic studies of the Chinese vascular plant flora and other studies at the intersection of systematics, evolution, biogeography, and functional and community ecology. One of the fundamental goals of systematics research is to transform knowledge gained through phylogenetic reconstructions into a predictive and stable classification system, reflecting the evolutionary histories of taxa for the use of the scientific community and the public (Wen et al., 2017, 2018; Funk, 2018; Le et al., 2018). Increasingly, robust phylogenies based on extensive or complete sampling of species derived from analyses of genomic data are available to serve as the basis for classification. In this issue, Wang et al. (2020b) present a revised classification of Magnolia L. and the Magnoliaceae, based on results from phylogenomic analyses of plastid genome sequences from genome skimming with broad taxon sampling. Similarly, Ye et al. (2020) conducted a phylogenetic study of Diapensiaceae using chloroplast genome data and a broad sampling of Diapensia L. to address the status of several species. Su et al. (2020) applied a novel collection-based phylogenomic approach to clarify species boundaries in the Stachyuraceae, a family endemic to eastern Asia. Collection-based molecular approaches allow extensive taxonomic sampling without the time and expense of visiting geographically disparate field sites. Such studies enable simultaneous study of morphologically distinguishing characteristics for resolved clades in the phylogeny (Willis et al., 2017). All three studies (Hu et al., 2020; Su et al., 2020; Ye et al., 2020) clarified previous taxonomic debates in these taxa and enabled the authors to propose revised taxonomic treatments based on a large amount of molecular phylogenetic data. Furthermore, the phylogeny of Magnolia, in particular, provides a comprehensive framework that may prove useful in breeding programs in this horticulturally important genus. The authors of all three papers further elucidated the diversification in space and time of these taxa via biogeographic and divergence time analyses. The basis for transforming phylogenetic data into classification systems lies in the definition of species and species delineation. Although many species concepts have been proposed, delineating species remains a major challenge in taxonomy and is an active topic of research in systematics. In this issue, Hong (2020) proposes an explicit statistics-based gen-morph species concept to bridge the genetic and morphological properties of species and to offer a species concept that is easily operable in taxonomic work. On the basis of findings from outcrossing in Paeonia L., Hong argues that species delimitation of outcrossing organisms can be accomplished by detecting statistical discontinuity of two independent morphological traits. Hong verifies that discontinuities in morphological features in outcrossing organisms such as Paeonia can be a good proxy for genetic distinction among species. This concept may facilitate morphology-based classifications, reflecting phylogenetic and genetic distinction in other outcrossing plants. A Brief Memorial Biography of the Late Prof. Tang Yan-Cheng (7 July 1926–6 August 2016). Prof. Tang (surname) Yan-Cheng (given name) (汤彦承, abbreviated Y. C. Tang in taxonomic citations) was born in Xiaoshan, Zhejiang Province, China. He graduated from Tsinghua [Qinghua] University in August 1950 and joined the Institute of Plant Taxonomy (now the Institute of Botany) of the Chinese Academy of Sciences. From October 1958 to October 1960, he was a visiting scholar at the Komarov Botanical Research Institute in Moscow, in the former Soviet Union. From 1972 to 1981, he was director of the Department of Plant Taxonomy and Biogeography in the Institute of Botany. As one of the key organizers of the state projects Iconographia Cormophytorum Sinicorum (Illustrated Vascular Plants of China) and Flora Reipublicae Popularis Sinicae (FRPS), he wrote and edited several of the volumes in those two important series of books. He received the National Natural Science First Prize (one of two winners, with Prof. Wang Wentsi) for the former and the National Natural Science Third Prize for the latter. Through his own research and other professional activities, he actively promoted the advancement and prosperity of plant taxonomy, plant systematics, and phytogeography in China. He was a versatile and knowledgeable scholar, and a well-known and excellent mentor and friend in the Chinese plant taxonomy community. He excelled in his knowledge of classic literature, botanical nomenclature and botanical Latin, species concepts, and cladistics. He paid close attention to the latest international developments in plant taxonomy/systematics and introduced new ideas, theories, and methods to his Chinese colleagues and to the Chinese botanical community in a timely manner. Those endeavors had a significant impact on the development of modern plant taxonomy/systematics in China. Prof. Tang developed a broad, diverse base of knowledge through his education. From 1942 to 1945, Tang attended Suzhou Taowu Middle School, a private institution in Shanghai. Due to the influence of his Chinese teacher, Wang Bingliu, from that school, Tang advocated the ideals of the “Seven Wise Men in the Bamboo Forest (竹林七贤),” a group of Chinese scholars, writers, and artisans of the third-century CE who followed Taoism, which essentially promoted living in harmony with nature. In his later years, Tang enjoyed Zhuangzi (庄子), a collection of writings from the fifth to third century BCE that were a fundamental influence on the development of Taoism. In 1945, he entered the College of Agriculture at St. John's University in Shanghai, a private university, for undergraduate study. Later, he transferred to the Advanced Class at Shanghai Temporary University. In October 1946, he was recommended and admitted to Tsinghua University, which was and remains one of China's top universities. Of all biology students at Tsinghua at the time, he was the only one who chose to major in botany. As a student of botany, he studied plant taxonomy with Wu Zhengyi (Wu Cheng-yih) (1916–2014) and plant morphology and systematics with Prof. Zhang Jingyue (1895–1975). The teachings of Wu Zhengyi and Zhang Jingyue, which were complementary, interactive, and guiding, not only inspired Tang Yan-Cheng in plant taxonomy, but also instilled in him an exceptional capacity for self-learning and the habit of thinking outside taxonomy and absorbing ideas from other disciplines. The teacher–student friendship that Tang Yan-Cheng developed with Wu Chengyi during Tang's four years as a student at Tsinghua led to a half century of collaboration between these two famous Chinese plant taxonomists. Prof. Tang admired the following remark by the famous Chinese historian Mr. Fan Wenlan (1893–1969): "板凳要坐十年冷, 文章不写半句空 (Literally: the bench has to sit cold for ten years, with no wasteful words in the written article)". The real meaning may be to sit on the cold bench for ten years to concentrate on the pursuit of truth before putting pen to paper. Notably, Professor Tang did not publish as many papers as his peers, but his work was novel, thoughtful, influential, and highly regarded. He did not spend time dwelling on ideas that were out of date (Wang et al., 2020a). He continued his work with undiminished rigor until his last breath. Prof. Tang was knowledgeable, modest, and easy-going, and he was selflessly dedicated to plant taxonomy throughout his life. He was a humble and honorable person who worked tirelessly and quietly to enhance the development of plant taxonomy in China. He never sought honors or attention for himself, but instead always tried to help and promote others. His contributions to plant taxonomy and scientific research, as well as his moral character, will continue to inspire not only those of us who were privileged to know him, but future generations in China as well. A more detailed biography of Prof. Tang is available in the study of Wang et al. (2020a) where specific contributions of Prof. Tang to Chinese botany are discussed. We thank AJ Harris and Jun Wen for reviewing and providing constructive editing and comments on the article. We also thank JX Wang, HN Qin, and AM Lu for contributing information on Prof. Tang's biography and JSE journal manager Y Liang and the chief editors J Wen and S Ge for their support.