INTEGRATING TAXONOMY, EVOLUTIONARY BIOLOGY, GENETICS, AND FUNCTIONS TO UNDERSTAND BIODIVERSITY IN DOGWOODS AND OTHER PLANTS AT MULTIPLE DIMENSIONS

• Sponsoring Institution: National Institute of Food and Agriculture
• Project Status: COMPLETE
• Funding Source: HATCH
• Reporting Frequency: Annual
• Accession No.: 1001502
• Project Start Date: Dec 9, 2013
• Project End Date: Sep 30, 2018
• Program Code: [(N/A)]- (N/A)

Recipient Organization
NORTH CAROLINA STATE UNIV
(N/A)
RALEIGH,NC 27695

Performing Department
Plant Biology

Non Technical Summary
Much of the Earth's biodiversity has remained uncharacterized and poorly understood, but is being lost at an alarming rate. A full understanding of biodiversity, especially its origin, evolution, and impact across multiple dimensions and environments, is an eminent task in the 21st Century and is vital to conserving and sustaining the Earth's biota. The primary goal of the project is to enhance our understanding of origin and evolution of angiosperm biodiversity at different levels, from clades, species, to morphology, genomes and genes, as well as functional traits from a phylogenetic perspective. During this project period, the study will focus on the Cornales (the dogwoods and close relatives) and other groups of horticulture importance. The dogwood family and relatives (order Cornales, ~ 500 species, worldwide) contain plant elements that are both economically and ornamentally important. Common representatives include Cornus florida (flowering dogwood ), C. kousa (kousa dogwood), C. canadensis (bunchberry ), C. mas (European cornelian cherry ), C. sericea (red osier dogwood ), Davidia involucrata (dove tree), Hydrangea macrophylla (Hydrangea), Deutzia spp. (deutzias), and Philadelphus spp. (mock oranges), which are widely cultivated as ornamental plants. Several species are medicinally important, including Cornus officinalis (cornelian cherry), Camptotheca accuminata (Happy tree), Curtisia dentata (assegai tree), and Alangium salvifolium (sage-leaved alangium). The group is morphologically heterogeneous and has a cosmopolitan distribution, occurring from cold temperate regions to the tropics, rarely in subarctic zones. Many members have restricted, modern geographic distributions, but having fossils occurring in areas outside their present distribution. This pattern of geographic distribution and variation in morphology make the order a model for studying the generation and evolution of biodiversity at the different levels, and for addressing a variety of ecological, evolutionary, and biogeographic questions. In this phase of the project, we are focusing on the following three objectives: 1)The molecular basis of inflorescence evolution in the dogwood genus (Cornus L., Cornaceae, Cornales), 2)Evolutionary and population genetics of Cornus florida (Cornaceae), and 3)Phylogenetic relationship, biogeography, and species delineation in taxa of Cornales and other plants from eastern North America and eastern Asia. A multiple disciplineary approach integrating taxonomy, evolutionary biology, and genetics will be employed to address these questions. The study will shed new light into the origin and evolution of biodoversity in these non-model plant lineages at both species and molecular levels and advance our understanding of genetic controls of inflorescence evolution in angiosperms.

Animal Health Component

(N/A)

Research Effort Categories

Basic

90%

Applied

(N/A)

Developmental

10%

Classification

Knowledge Area (KA)	Subject of Investigation (SOI)	Field of Science (FOS)	Percent
206	2110	1060	100%

Knowledge Area
206 - Basic Plant Biology;

Subject Of Investigation
2110 - Ornamental trees and shrubs;

Field Of Science
1060 - Biology (whole systems);

Keywords

phylogenetics

biogeography

developmental genetics

inflorescence

cornus

cornales

Goals / Objectives
The major goal of the project is to building robust phylogenies of dogwoods and related taxa using molecular data and use the phylogenies as the comparative framework to understand the origin and evolution of biodiversity at different levels, from clades, species, morphology, genes, and genoomes.

Project Methods
Approaches from systematics, biogeography, population genetics, evolutionary developmental genetics will be integrated to understand the molecular basis underlying the evolution of inflorescence evolution and divergence in the dogwood genus. Gene cloning, comparative analyses of gene expression using qRT-PCR and in-situ hybridization, comparative analyses of functions of candidate genes using genetic transformation, and phylogenetic and molecular evolutionary analyses of candidate genes will be applied in the study. Next generation sequencing based RADseq and targeted enrichment sequencing will be used to generate genomic scale molecular data for phylogenetic and population genomic analyses of study taxa. Metabolomic profiling will be used to fingerprint the secondary compounds in C. florida. The results will be compared among species and/or populations from a phylogenetic perspective to understand the evolutionary changes of traits, distribution ranges, and molecular mechanisms driving morphological divergence. The results will be disseminated to the community via publication in peer-reviewed journals, presentation at conferences, and invited seminars, as well as in-classroom teaching.

Progress 12/09/13 to 09/30/18

Outputs
Target Audience:Scientific communities in systematics, evolutionary biology, evolutionary ecology. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?One PhD student, one technician, three visiting scientists (associate professors), and two undergraduate obtained training in plant development, molecular phylogenetics, and evolution. How have the results been disseminated to communities of interest?Results were published in journal articles or presented at national professional conferences or at invited siminars. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Functional analysis of CorTFL1 gene using genetic transformation experiments confirmed the role of the gene in regulating flowering time and inflorescence initiation and morphology. Changes of phylotaxy in a few transgenic plants with CorTFL1 down-regulated or CorLFY upregulated were also observed, suggesting functions of CorTFL1 in regulating phylotaxy through anagonistic interactions with CorLFY gene. However this function needs to be confirmed with additional experiments. The evidence, together with the expression patterns of these genes (CorTFL1, CorAP1, and CorLFY) among species support role of them in the evolution of of inflorescence architecture and origin of head and umbels in Cornus. Phylogenomic study using plastid genome data for Cornales resolved a strongly supported phylogeny of the order revealing relationships among families consistent with those found in my previous study based on a few plastid genes (manuscript in review). However, the plastid genome phylogeny revealed novel relationships within the big-bracted dogwood group, revealing Cornus nuttallii in western North America diverging out first, followed by the Mexican C. disciflora, and C. florida is sister to the Asian big-bracted dogwoods (C. kousa, C. capitata, C. hongkongensis,etc.). These relationships are moderately to strongly supported and are not consistent with those found from analysis of nuclear data from RAD-seq (manuscrpit in prep). The RAD-seq data-based phylogeny of the Big-Bracted dogwoods strongly supported that C. florida and C. disciplora are sisters, which are in turn sister to the Asian big-bracted species. The causes of this conflit will be a consequence of rapid early diversification of the group in America. Phylogenomic study of Nyssa sylvatica complex resolved relationship within the group and supported recongnition of two species and down ranking N. ursina to a subspecies of N. biflora. The two species was esimated to diverged in the Miocene. Using DNA sequence data of 38 nuclear genes, we generated the first molecular phylogeny of Nyssa genus. The phulogeny and molecular dating analysis indicated an early divergence of the Central Amercan N. talamacana in the Eocene and rapid raditation of the genus into three major lineages in the early Eocene. Using genome-wide DNA data from RAD-seq, phylogenies of Aesculus, Hamamelis, Torreya, and Castanea were reconstructed. The biogeographic histories, niche evolution, and morphological trait evolution were examined. Manuscript for Aesculus is in preparation. Results from integrative analysis of genetic and metabolite diversities for Cornus florida was published. The study identified a group of secondary compounds that are associated with loci under selection and with plant health. Comparataive analyses of putative single copy orthologous genes in 20 species pairs revealed a common pattern of gene evolution - relative abundance of genes underly different levels of natural selectoin force is conserved among species pairs. More than 200 genes were identified to be under positive selection; some of which were annotated to functions in biological process responding to biotic or abiotic stimuli.

Publications

• Type: Journal Articles Status: Published Year Published: 2019 Citation: Liu, X*, J Zhang, DY Xie, RG Franks, Q-Y(J) Xiang1#. 2019. Functional characterization of Terminal Flower1 homolog in Cornus canadensis by genetic transformation. Plant Cell Report. https://doi.org/10.1007/s00299-019-02369-2.
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Zhou*, W, J Xiang, S Obata*, A Pais*, Y Dong*, R Peet#, Q-Y(J) Xiang#. 2018. Resolving relationships and phylogeographic history of the Nyssa sylvatica complex using data from RAD-seq and species distribution modeling. Molecular Phylogenetics and Evolution, 126, 1-16. DOI: 10.1016/j.ympev.2018.04.001
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Pais*, AL, X Li (S), and Q-Y(J) Xiang#. 2018. Discovering variation of secondary metabolite diversity and its relationship with disease resistance in Cornus florida L. Ecology and Evolution. 8 (11). DOI: 10.1002/ece3.4090.
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Nowicki, M, SL Boggess, AM Saxton, D Hadziabdic, Q-Y(J) Xiang, T Molnar, Y Zhao, RN Trigiano. 2018. Haplotyping of Cornus florida and C. kousa chloroplasts: insights into species-level differences and patterns of plastic DNA variation in cultivars. PLOS ONE. Volume & Issue: 13 Page Number(s): e0205407.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Liu*, X, L Li*, and Q-Y(J) Xiang#. 2017. Down regulation of APETALA3 homolog resulted in defect of floral structure critical to explosive pollen release in Cornus Canadensis. Journal of Systematics and Evolution. doi: 10.1111/jse.12272.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Ma Q*#, W Zhang, and Q-Y(J) Xiang# 2017. Evolution and developmental genetics of floral displayA review of progress. Journal of Systematics and Evolution. doi: 10.1111/jse.12259.
• Type: Journal Articles Status: Under Review Year Published: 2019 Citation: Fu, C-N, Z-Q Mo, J-B Yang, X-J Ge , D-Z Li# , Q-Y (J) Xiang#, L-M Gao#. Under review. Plastid phylogenomics and biogeographic analysis support a wide spread ancestor northern hemisphere origin and rapid early divergence of Cornales in the Mid-Creaceous time. Molecular Phylogenetics and Evolution .
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: . Liu, X, D Xie, R Franks, Q-Y(J) Xiang. Functional Characterization of Terminal Flower1 Homolog (CorTFL1) in Cornus canadensis Deciphering its role in evolution of Inflorescences in Cornus. BSA conference (Botany 2018), Rochester, MN. July 21-25.
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Zhou, W, Q-Y(J) Xiang, and J Wen. Phylogenomics of Nyssa from single copy genes and Fluidgim sequencing  insights into biogeography and character evolution. BSA conference (Botany 2018), Rochester, MN. July 21-25.
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Zhiyuan Du, AJ Harris, and Q-Y(J) Xiang. Phylogenomics of the tribe Hippocastaneae (Sapindaceae) inferred from RAD-seq data - insights into biogeography and evolution of the genus Aesculus L. BSA conference (Botnay 2018), Rochester, MN. July 21-25.
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Zhou, W. Species delineation & phylogenetics in an eastern Asia-eastern North America disjunct genus Nyssa. 1st NCSU Genomics and Bioinformatics joint symposium. April 6-7. Hunt Library, Centennial Campus, NCSU.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: 8. Ma*, Q, X Liu*, RG Franks#, QY(J) Xiang#. 2017. Alterations of CorTFL1 and CorAP1 expression correlate with major evolutionary shifts of inflorescence architecture in Cornus L. (Cornaceae)  a model for variation of determinate inflorescences. New Phytologist. DOI: 10.1111/nph.14197.
• Type: Journal Articles Status: Other Year Published: 2019 Citation: Dong, YB+, SC Chen+, SF Cheng, WB Zhou, Q Ma, ZD Chen, CX Fu, X Liu#, YP Zhao#, PS. Soltis#, G Wong#, DE. Soltis#, Q-Y (J) Xiang+#. Natural selection and repeated genomic patterns of functional genes following allopatric speciation in eastern Asian-eastern North American disjunct plants. eLife. Review returned; In revision for resubmission.

Progress 10/01/16 to 09/30/17

Outputs
Target Audience:Reached audience: Plant scientist, taxonomist, evolutionary biologists, and college students in biology, natural resources, and evironmental sciences. Efforts: publication of research results in national and international journals of plant sciences; research presentations at regional, national and international conferences; lectures to college students. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project provided research opportunities for training and/or career development of 3 Ph.D.students, 1 undergraduate student, 1 professional technician, and 1 visiting faculty in the reporting period. Through classroom teaching and study abroad course, the project outreached ~75 students, staff, and faculty and provided training in botany. How have the results been disseminated to communities of interest?Mainly through publication of research papers in journals, oral and poster presentations at regional, national, and international conferences, workshops, and symposia. Part of resuls were also disseminated via classroom lectures. What do you plan to do during the next reporting period to accomplish the goals?For year of 2017-2018, my plan is to focus on understanding the species relationship, biogeographic history, and trait evolution of the disjunct tree genera Nyssa, Hamamelis, Aesculus, Castanea, Cornus, and Torreya using a phyloggenomic approach. Efforts would also be devoted to complete the Cornales phylogenomic analyses and publish research results from previous year's work, incluiding and present results at the conferences.

Impacts
What was accomplished under these goals? Phylogeny-based analyses of gene expression among dogwood species (Cornus) suggested alteration of expression patterns of CorTFL1 and CorAP1 during early development of inflorescences is important to the evolutionary changes of inflorescence architecture in Cornus. -resultes were published. Phylogeny-based analyses of transcriptome sequences revealed ancient genome duplication in common ancestor of Cornus. - Results were published. Functional analysis of petal identify gene CorAP3 in bunchberry (Cornus acanadensis) using agrobacterium-mediated genetic transformation technology was done. Results indicated that down-regulation of the gene resulted in the loss of a floral structure critical to explosive pollen release that uniquly evolved in the herbaceous dogwood members of Cornus. -Results were published. Conducted field test of SOR plants for heat tolerance in natural condition in North Carolina. Results were inclusive due to mild summer, a shady environment, and root disease. Landscape ecological genomics study on Cornus florida (the flowering dogwood tree) found evidence of local adaptation and 54 loci were identified as strong candidates for adaptation to different environmental variables and some were associated with plant disease condition. -Results were published. Integrative analysis of genetic and metabolomic diversities for Cornus florida identified a group of secondary compounds that are associated with loci under selection. - Manuscript was under preparation. Phylogenomic study of Nyssa sylvatica complex (Nyssaceae, Cornales) in eastern North American resolved relationships within the clade. We found strong evidence supporting two species N. sylvatica and N. bilfora, with two subspecies within N. bilflora. A former species N. ursina was down-ranked to a subspecies of N. biflora. -- Manuscript was under preparation. DNA sequence data for 38 nuclear single copy genes were obtained for phylogenomic study of Nyssa genus. Phylogenetic analysis was completed. DNA sequence data for the blue- or white-fruited dogwood group were generated using RAD-seq approch and data were analyzed. DNA libraray for gene target enrichment sequencing were prepared for all Cornales taxa. Analyses of molecular evoultion of data from transcriptome sequences of 22 genera disjunctly distributed in eastern Asia and eastern North America was conducted. Field work was conducted to collect leaf samples and DNAs were extracted from the samples of the target tree genera disjunctly distributed in eastern Asia and North America.

Publications

• Type: Book Chapters Status: Awaiting Publication Year Published: 2017 Citation: GR.Plunkett, QY(J) Xiang, G Schutzs. Toricelliaceae. In: The Families and Genera of Vascular Plants (ed. K.Kubitzki). Vol. X. Asteridea (vol. Ed. J. W. Kadereit). In press.
• Type: Journal Articles Status: Published Year Published: 2016 Citation: Liu*, X, J Zhang*, A Abuahmad, RG Franks#, D-Y Xie#, QY(J) Xiang#. 2016. Analysis of TFL1 homologs in dogwood species (Cornus L.) indicates functional conservation in control of transition to flowering. Planta. 243:1129-41. doi: 10.1007/s00425-016-2466-x.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Geng*, XM, X Liu*, M Ji, WH, A Grunden# and QY (J) Xiang#. 2016. Enhancing heat tolerance of the little dogwood Cornus canadensis L. f. with introduction of a superoxide reductase gene from the hyperthermophilic archaeon Pyrococcus furiosus. Frontiers in Plant Sciences. Vol 6, article 26;| http://dx.doi.org/10.3389/fpls.2016.00026.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Yu, Y*, QY(J) Xiang*, P Manos, DE Soltis, PS Soltis, BH Song, SF Chen, X Liu, G Wong. 2017. Whole genome duplication and acceleration of molecular evolution is associated with the early diversification of the genus Cornus L. (Cornaceae): Insights from De Novo Assembled Transcriptome Sequences. PLoS ONE 12(2): e0171361. https://doi.org/10.1371/journal.pone.0171361
• Type: Journal Articles Status: Published Year Published: 2016 Citation: Harris, AJ, CX Fu, QY(J) Xiang, LaRinda Holland, Pedro Acevedo, and J Wen. 2016. Testing the monophyly of Aesculus L. and Billia Peyr, wood genera of tribe Hippocastaneae of the Sapindaceae. Molecular Phylogenetics and Evolution. 102:145-51. doi: 10.1016/j.ympev.2016.06.001. Epub 2016 Jun 3.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Ma*, Q, X Liu*, RG Franks#, QY(J) Xiang#. 2016. Alterations of CorTFL1 and CorAP1 expression correlate with major evolutionary shifts of inflorescence architecture in Cornus L. (Cornaceae)  a model for variation of determinate inflorescences. New Phytologist. DOI: 10.1111/nph.14197.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Pais* AL, RW Whetten, and Q-Y(J) Xiang. 2016. Ecological genomics of local adaptation in Cornus florida L. by Genotyping by Sequencing. Evolution and Ecology. doi: 10.1002/ece3.2623. 2017 Jan; 7(1): 441465.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Liu, X, L Li, and Q-Y(J) Xiang*. 2017. Down regulation of APETALA3 homolog resulted in defect of floral structure critical to explosive pollen release in Cornus Canadensis. Journal of Systematics and Evolution. doi: 10.1111/jse.12272.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Ma Q*, W Zhang, and Q-Y (J) Xiang* 2017. Evolution and developmental genetics of floral displayA review of progress. Journal of Systematics and Evolution. doi: 10.1111/jse.12259.
• Type: Theses/Dissertations Status: Published Year Published: 2017 Citation: Molecular Characterization of Local Adaptation of Natural Flowering Dogwood Populations (C. florida) to Fungal Pathogens and Environmental Stress.
• Type: Book Chapters Status: Published Year Published: 2016 Citation: 1. Xiang, QY(J). 2016. Aucubaceae. In: The Families and Genera of Vascular Plants (ed. K.Kubitzki). Vol. XIV. Flowering Plants. Eudicots (vol. Ed. J. W. Kadereit, Volker Bitterich). P 37-40. Springer Nature, AG Switzerland.
• Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Wenbin Zhou, Sirius Li, and Qiu-Yun(Jenny) Xiang. Understanding functional diversity and mechanisms of plant community assembly using non-target metabolite profiling: a test of HPLC-MS method. XIX International Botanical Congress, Shenzhen, China. July.
• Type: Book Chapters Status: Published Year Published: 2016 Citation: 2. Xiang, QY(J). 2016. Helwingiaceae. In: The Families and Genera of Vascular Plants (ed. K.Kubitzki). Vol. XIV. Flowering Plants. Eudicots (vol. Ed. J. W. Kadereit, Volker Bitterich). P213-216.
• Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Comparative and functional genomics in Cornus. In symposium Advances in genomic analyses and genetic modification technologies for woody horticultural species. American Society of Horticultural Sciences annual conference. Haiwaii.

Progress 10/01/15 to 09/30/16

Outputs
Target Audience: Nothing Reported Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project provided research opportunities for training and/or career development of 4 undergraduate students, 3 Ph.D. students (1 was a visiting student from China), 1 postdoctoral students, 2 professional technician, and 2 visiting faculty members from China. Through classroom teaching and study abroad course, the project outreached ~30 people and provided training in botany. How have the results been disseminated to communities of interest?Through classroom lectures on Systematic Botany, and study abroad course and other activities performed by graduate students listed below: • As participant in departmental science partnership with local elementary schools • As Botanical Society of America Public Policy Representative advocating science policy to US Congress •Led guided hikes of conserved lands with Triangle Land Conservancy (Temple Flatrock, Flower Hill, Brumley Preserve) and assisted with Bio Blitzes (Walnut Hill) •Organized and spoke in science panel promoting STEM careers for community college students. What do you plan to do during the next reporting period to accomplish the goals?My research goals are to maintain a productive research program in plant systematics and evolution via collaborative research. The focus for 2016 will be in three main areas: Evolutionary developmental genetics of inflorescence evolution in dogwoods. NSF support to the project will end in August. I have submitted pre-proposal to NSF for funding to support continuous research of the project. The long term goal of the research is to unravel the developmental and genetic controls governing the inflorescence architecture divergence among dogwood species. Results from the research have broad implications to understanding and manipulating horticultural and agriculture crops. The research activities in 2015 resulted in a number of transgenic plants of Cornus Canadensis in flower, allowing analyses of phenotypes that is on-going. In 2016, efforts will be devoted to publication of more results from gene expression and functional analyses. Additional transgenic lines and plants will be generated to provide statistical power to phenotype analyses. Maintaining cultures of the SOR heat-tolerant bunchberry plants that we filed a technology transfer (plant disclosure) for potential horticultural uses. Effort will be made obtain permit for field testing of the plants. 3) Phylogenomics of eastern Asian-eastern North American disjunct tree genera and community phylogenomics of eastern Asian-eastern North American disjunct forests. The research is a component of the collaborative NSF Dimensions of Biodiversity project newly funded in 2015. Efforts will be devoted to field collections of samples and DNA extractions of large number of samples, as well as primer design of phylogenetic markers. A new graduate student has been recruited to start in the fall. 4) Phylogeography and population ecological genomics of C. florida natural populations. This is a part of the collaborative grant "Developing Flowering Dogwood as a Focal Genomic Resource for Woody Ornamentals", funded by NSF. Efforts will be made to complete the GBS data analyses, presentation of results at meetings, and manuscript preparation. 5) Phylogenomics and evolution of Cornales and other plants. This is also a part of the dogwood genome project funded by NSF. Efforts will be focused on developing phylogenetic markers using target enrichment approach to capture 300 low copy nuclear genes for phylogeomic analyses. DNAs for over 300 samples have been prepared. Effort will be made to obtain materials for a few missing species that are critical to the study. A postdoc has been recruited to work on this project. 6) Efforts will be devoted to publishing the manuscripts in preparation for Nyssa, Cornus florida, and others worked on by former visiting students and scholars not listed above. Effort will also be made to organize the BSA symposium funded by BSA and JSE at the BSA conference, and to present our results at this and other conferences.

Impacts
What was accomplished under these goals? Issues: 1.Angiosperms (flowering plants) dominate most terrestrial and semiaquatic habitats and are unimaginably important to humankind. The flower organization () in angiosperms is primarily important to flowering plant reproduction. Variation in inflorescence architectures affects the success of plant reproduction and the yield of a crop by influencing seed number and dispersal/harvest ability. Despite the importance of inflorescence innovation in angiosperm evolution and crop production, we know little about the genetic basis of inflorescence development and the molecular changes that have altered inflorescence constructions in different plant lineages. 2. Biodiversity is multidimensional, composed of genetic, phenotypic, ecological, and geographic variation within and among species. Understanding the sources and patterns of Earth's biodiversity will lead to better understanding of our planet's ecosystems and how to conserve them.Within forests, plants grow in association with soil microbes and both are major players determining ecological functions of a plant community. However little is known about the factors determining biodiversity at different levels, how biodiversity of plants and microbes affect each other, how biodiversity affects ecosystem functions, and how evolutionary history influences the biodiversity assembly in a forest. The forests of eastern Asia and eastern North America were once connected in the Tertiary and shared an evolutionary and ecological history; they therefore offer an excellent opportunity to study these questions and uncover the drivers of biodiversity across geographic space and through evolutionary time. 3. .Protecting rare species from extinction is critically important. Information on genetic diversity and its spatial distribution, and breeding systems of rare or endangered species is essential to conservation managing strategies. The NC state flower, Cornus florida L., is being threatened by many fungal pathogens of which dogwood anthracnose is most severe. Recent surveys of natural populations of C. florida indicated a 48 to 88 percent decrease in population within the southern Appalachian mountain region, raising a concern on the long-term survival of the species. 4.Polyploidy is an important mechanism in plant speciation that generates biodiversity and major resources of wild progenitors of agriculture crops. However, origin of polyploidy species and genetic consequences following genome duplication remain poorly understood in most plant groups. Such information is essential to breeding, conservation, and evaluating of sustainability of crops and biodiversity. What have been done: Issue 1. The dogwood genus Cornus L., contains many popular garden plants and the NC state flower C. florida. This genus provides an excellent model for studying the genetic basis underlying the modification of inflorescence architectures due the variation in inflorescence morphology among species. NCSU plant molecular systematist Jenny Xiang uses the genus as a model and works with collaborators to unravel the developmental and molecular mechanisms responsible for the origins of different inflorescence types. An agrobacterium-mediated genetic transformation system has been developed for the model dogwood species Cornus canadensis, and a number of transgenic plants with up- or down-regulation of candidate genes known to control inflorescence development in Arabidopsis have been generated for evaluating their roles. The expression patterns of these genes in floral and inflorescence development have also been investigated for different species. Screening and characterization of additional candidates are in progressing. Issue 2. NCSU plant systematist, Jenny Xiang and her research group is a part of a multiinstitutionalteam focusing on phylogenetic and biogeographic study of tree genera occurring in eastern Asia and North America (Hamamelis, Castanea, Aesculus, Torreya, and several groups withinCornales order). Xiang and her colleagues have gathered DNA materials for most of the species and are developing new markers for phylogenomic analyses. The phylogenomic analyses are expected to provide robustphylogeniesfor testing biogeographic and evolutionary hypotheses. Issue 3. NCSU plant systematist Jenny Xiang and her graduate students are investigated genetic diversity of the flowering dogwood tree Cornus florida. The study applies next generation sequencing technology and combines ecological niche modeling and analyses of environmental variables and functional traits to gain insights into the evolutionary history of the species and the molecular markers likely linked to local adaptation and disease resistance. Issue 4. NCSU plant systematist Jenny Xiang is working with horticultural scientist Tom Ranney, and forest geneticist Ross Whetten for a phylogenetic study of Fothergilla in the witch hazel family using molecular data generated from next generation sequencing technology. Fothergilla is a popular nursery ornamental genus consisting of polyploidy species and newly discovered diploid populations. The research shed light on the evolutionary origins of the polyploidy species and their relationships to the diploid populations. Xiang's lab is also working on the dwarf dogwood group that consists of a mix of diploid, tetraploid, and hybrids taxa using phylogenetic analyses of DNA sequence data to test the hypothesis of hybrid origin of the polyploid species. Impact: Systematic and evolutionary studies of Cornales and Fothergilla address fundamental issues of population biology, systematics and biodiversity that are needed to understand the mechanisms of biological adaptation, speciation, and evolution. The research also addresses the crises brought about by the concomitant depletion of biological diversity and the dwindling taxonomic expertise necessary to study and preserve the earth's biota. Our molecular systematics research on Cornales and genetic analysis of Cornus florida, and phylogenomic studies of Fothergilla contribute to the developing emphasis on discovery and preservation of genomic diversity on these plants that hold enormous horticulture value in the world. Furthermore, identification of genetic changes leading to the innovation of inflorescence architectures in Cornus will not only shed light on how evolution of developmental and genetic programs shaped the morphology of inflorescence architectures in angiosperms, but also hold a promise in bioengineering of dogwoods to produce plants with novel inflorescence forms or other traits for ornamental purposes. Using our genetic transformation system, we successfully generated trangenic Cornus canadensis plants that are early flowering or heat. The species has no close relatives in the south that may potentially hybridize with, thus escape of heat tolerant gene SOR to wild relatives is not a concern. The transformed species would provide the source material for industrial production of new variety of ground cover plants in the south. The research on wild resources of Fothergilla and Cornus florida directly contributes to the conservation of these species with great ornamental value and guide genetic breeding for new cultivars.

Publications

• Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: 5. 2016 Dong, Y, J Li, G K-S Wong, DE Soltis, PS Soltis, and Q-Y (J) Xiang. Patterns of morphological and molecular divergence of species pairs between eastern Asia and eastern North America inferred from transcriptome data. 2016 Botany Conference, Savannah, GA.
• Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: 6. 2016. Pais, A, (QY) J Xiang, P Wadl, J. Population genetics meets ecological genomics and community ecology in C. florida. 2016 Botany Conference, Savannah, GA.
• Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: 7. 2016. Liu, X, D Xie, R Franks, QY (J) Xiang. Down- regulation of AP3 homolog expressions showed resulted in loss of the floral and inflorescence changes leading to loss of for the explosive pollen release in bunchberry (Cornus canadensis). 2016 Botany Conference, Savannah, GA.
• Type: Journal Articles Status: Published Year Published: 2015 Citation: 1. Call1, A, YX Sun4, Y Yu4, P Pearman, R Trigiano, DT Thomas, I Carbon, and QY(J) Xiang*. 2015. In revision. Population structure and Pleistocene biogeography of Cornus florida L. (Cornaceae) - integrating phylogeography and ecological niche modeling. Journal of Systematics and Evolution. DOI: 10.1111/jse.12171.
• Type: Journal Articles Status: Published Year Published: 2015 Citation: 2. Qi4, ZC, Y Yu4, X Liu3, A Pais1, T Ranney*, R Whetten*, and Q-Y (J) Xiang*. 2015. Phylogenomics of polyploidy Fothergilla (Hamamelidaceae) by RAD-tag based GBSInsights into species origin and effects of software pipelines. Journal of Systematics and Evolution. DOI: 10.1111/jse.12176.
• Type: Journal Articles Status: Published Year Published: 2016 Citation: 3. Geng4, XM, X Liu3, M Ji, WA Hoffmann, A Grunden* and QY (J) Xiang*. 2016. Enhancing heat tolerance of the little dogwood Cornus canadensis L. f. with introduction of a superoxide reductase gene from the hyperthermophilic archaeon Pyrococcus furiosus. Front. Plant Sci., 29 January | http://dx.doi.org/10.3389/fpls.2016.00026.
• Type: Journal Articles Status: Published Year Published: 2016 Citation: 4. Liu, X, J Zhang, A Abuahmad, RG Franks*, D-Y Xie*, QY(J) Xiang*. 2016. Analysis of TFL1 homologs in dogwood species (Cornus L.) indicates functional conservation in control of transition to flowering. Planta. DOI :10.1007/s00425-016-2466-x.
• Type: Journal Articles Status: Published Year Published: 2016 Citation: 5. Harris, AJ, CX Fu, QY(J) Xiang, LaRinda Holland, Pedro Acevedo, and J Wen. 2016. Testing the monophyly of Aesculus L. and Billia Peyr, wood genera of tribe Hippocastaneae of the Sapindaceae. Molecular Phylogenetics and Evolution. Sep;102:145-51. doi: 10.1016/j.ympev.2016.06.001. Epub 2016 Jun 3.
• Type: Book Chapters Status: Published Year Published: 2016 Citation: 1. Xiang, QY(J). 2016. Aucubaceae. In: The Families and Genera of Vascular Plants (ed. K.Kubitzki). Vol. XIV. Flowering Plants. Eudicots (vol. Ed. J. W. Kadereit, Volker Bitterich). P 37-40. Springer Nature, AG Switzerland.
• Type: Book Chapters Status: Published Year Published: 2016 Citation: 2. Xiang, QY(J). 2016. Helwingiaceae. In: The Families and Genera of Vascular Plants (ed. K.Kubitzki). Vol. XIV. Flowering Plants. Eudicots (vol. Ed. J. W. Kadereit, Volker Bitterich). P213-216.
• Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: 1. 2016. Lindo, J, Y Dong, S Obata, X Ji, Q-Y(J) Xiang. Phylogenomic study of Blue/White-Fruited Dogwoods (Cornus, Cornaceae) using GBS data. NCSU Genomic Sciences Retreat, Carolina Beach, April 8-10th. 2016 Botany Conference, Savannah, GA. July 30  Aug. 3rd.
• Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: 4. 2016. Xiang, QY(J), Q Ma, X Liu, R Franks. A proposed TFL1-AP1-like gene-based model for the evolution of inflorescence architecture in Cornus L. (Cornaceae). 2016 Botany Conference, Savannah, GA. Talk at Symposium: Evolution, Development, and Genetics of Floral Display - Form, Size, and Arrangement. Symposium Organizer.

Progress 10/01/14 to 09/30/15

Outputs
Target Audience:College students via class lectures and field trips, high school student via summer research project, botany/plant biologists via seminars and conference presentations, university professors and administratorsfrom China via presentation, college alumini from China via presentation, and K-12 teachers from North Carolina via Duke Asian Pacific Study Workshop lecture and lab exercises. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project provided great opportunities for training and professional development of visiting scholars and graduate students during 2014-2015. Visiting Scholars: Dr. Xingmin Geng: training in methodology of molecular biology and manuscript writing.Drafted one manuscript on heat tolerant C. canadensis. Dr. Yan Yu: training in comparative and evolutionary analyses of transcriptome dataand molecular evolution andgenome evolution in dogwoods. Graduate Students: Ph.D. Andrew Pais - NCSU, training in population genomics approaches and manuscript writing. Ph.D. Julia Lindo - NCSU, training in phylogenetic analyses and taxnomy Ph. D. Qing Ma - visiting student,training in techniques applied toevolutionary developmental study of inflorescence evolution in Cornus, and manuscript writing.One manuscript has been prepared. MS. Xiaolong Zhang -visiting student, training in lab and computer techniques for molecular phylogenetics. Undergraduate students: Ashley Yew (female) -Transgenic plant nursing, DNA extraction and PCR. Shihori Obata (female) - training in molecular techniques (DNA extraction, electrophoresis, quantification, and phylogenetic analysis) Hign school student: Michael Yang - NC School of Mathematics and Sciences; Summer research projects on species distribution modeling. Research specialist/technition: Xiang Liu - training in molecular genetics, genetic transformationmanuscript preparation and writing. How have the results been disseminated to communities of interest?Conference papers and prepsentations at professionalconferences; lectures and labs in Plant Systematics courses taught, in study abraod courses from China. Lecure/presentation to universityadministrators from China Lecture/presentation to Sen Yat-sen University alumina group Workshop at Duke Asian Pacific Study to K12 teachers Manuscript publications in peer-reviewed journals What do you plan to do during the next reporting period to accomplish the goals?Continue analyses of phenotypes of transgenic plants and maintaining the cultures to flower. Generate additioanl transgenic lines to provide statistic support for the observed phenotypic effect obsorved. Work on revision of manuscripts for publication with additional data obtained. Work on generating molecular data for phylogenomics study of Cornales taxa. Conduct analyses of transcriptome data. Continue efforts in obtaining samples of Cornales and EA and ENA disjunct genera through herbarium visit and filed collecting. Expand study of C. florida to include more populations from across the distributional range using GBS method. Obtaining samples and generate the molecular data, and analyze the data.

Impacts
What was accomplished under these goals? The flower organization (inflorescence)is primarily important to angiosperm reproduction and crop yield by influencing seed number and dispersal ability. Despite the importance of inflorescence innovation, we know little about the genetic basis that is responsible for altering inflorescence constructions during angiosperm diversification. The dogwoods (Cornus L.) is a good system for such study due to variation of inflorescence architectures among species. Through comparative analyses of expression patterns and phenotypic effects, we addressed the roles of putative key inflorescence regulatory genes, CorTFL1, CorAP1, and CorLFY, in the evolutionary modification of inflorescences in Cornus. We foundvariation in expression patterns for CorTFL1 and CorAP1 were complementary to each other and correlated with inflorescence structures. Our genetic transformation experiments confirmed the role of these genes in regulating inflorescence development. The results shed new insights into thegenetic controlofinflorescence variationin dogwoods and maybe in angiosperms as whole.The genetic transformation system with the bunchberry hold a promise in bioengineering dogwoods to produce plants with novel inflorescence forms or other traits for ornamental purposes. Using this system,we obtained C. canadensis plants of early flowering or heat tolerant, providing potentialnew varieties for horticulture in warm regions. There is no dispute that phylogenetic relationships and population genetic structures are fundamental to the understanding, conservation, and utilizing biodiversity. These informationserves as the basis for testing hypotheses in speciation, biogeography, classification, and evolution, and provide guidance to conserving biodiversity and genetic breeding of agricultural and horticultural crops. Ourpopulation genomicsresearch onthe flowering dogwood treeCornus floridaand phylogenomic studies ofFothergillaand Cornalean taxa contribute to the developing emphasis on discovery and preservation of evolutionary andgenomic diversities of these plants that hold enormous horticulture value in the world.The research directly contributes to the conservation of these plants and guide genetic breeding for new cultivars. Objective 1. The molecular basis of inflorescence evolution in the dogwood genus (CornusL., Cornaceae, Cornales). 1) Completed experiments ofcomparing spatiotemporal expression patterns ofCorAP1andCorTFL1among dogwood species using in-situ hybridization and qRT-PCR and prepared manuscript for publication.The results showed the expression levels ofCorTFL1was strongly correlated with the branching level and branch elongation of inflorescences in early development and the expression level ofCorAP1was correlated with the inflorescence types inCornus. The expression levels ofCorTFL1andCorAP1were complementary to each other. 2) Monitoring experiments on creating an early flowering transformation system withCorcanFT and CorLFY over expressionand down regulation ofCorTFL1 and Investigating phenotypic effects of putative key inflorescence regulatory genes CorTFL1, CorLFY, and CorAP1 using genetic transformation experiments in C. canadensis. 3) Early flowering transgenic C. canadensis plants overexpressingCorLFYor with down regulation ofCorTFL1were developed. Some transformants with down regulation ofCorcanTFL1exhibited change of inflorescence structure while overexpression ofCorcanLFYresulted in no apparent inflorescence structural changes inC. canadensis. OverexpressingCorcanFTinC. canadensisdid not develop roots easily due to likely early maturation;flower-like structure in transgenic shoots during tissue culture were observed. Selected transgenic plants were analyzed to confirm transgene insertion and phenotypic effects. 4) Completeda manuscript validatingCorcanTFL1function and a manuscript reporting heat tolerant C. canadensis with SOR gene from archea. Manuscript was submitted. The key outcomesfrom gene expression andtransformation experimentssuggested thatCornusTFL1-like genes function to regulate the "vegetative" growth of inflorescences and that changes in the relative levels of CorTFL1 and CorAP1 expression in early inflorescence development may determine the evolutionary modification from large, elongated form to condensed, head-like or umbellate forms inCornus. This hypothesis is being tested with additional transformation experiments to generate more transgenic lines of C. canadensis. Objective 2. Evolutionary and population genetics ofthe flowering dogwood tree C. florida(Cornaceae). Cornus florida is threatened by fungal pathogens, especially by powdery mildew and dogwood anthracnose. The species is also subjected to abiotic environmental heterogeneities, such as variation in soil-nutrient composition and moisture, temperature, and length of growing season, across its natural distributional range in eastern North America. We genotyped 181 plants from six localities of North Carolina representing the coastal, Piedmont, and mountains habitats using GBS method (genotyping by sequencing). Analyses were conducted to identify single nucleotide polymorphism (SNP) outliers correlated with environmental variables and disease and to test if heterogeneity of abiotic pressures resulted in genetic differentiation indicative of local adaptation. The preliminary results showed 1) substantial (although not strong) genetic differentiation between coastal and Piedmont-Mountain subpopulations; 2) a list of 22 candidate loci putatively under selection, representing genetic signatures of local adaptation. Manuscript to publish the result was drafted. Comparative analyses of leaf secondary metabolite profiling were also completed for the 181 plants to identify SNP loci associated with chemical phenotypes and to assess whether chemical/phenotypic diversity is reflected by genetic diversity. The data will be used to explore if disease infected plants display differences in profiling of secondary metabolites. Objective 3. Phylogenetic relationship, biogeography, and species delineation in taxa of Cornales and other plants from eastern North America (ENA) and eastern Asia (EA). 1) Obtaining leaf samples and extracting DNAs for studies of Cornales species and other taxa occurring in EA and ENA via collecting in the field or botanical gardens. Focuses were Cornus, Nyssa, and flowering plant genera with two or a few species confined in EA and ENA. 2) Collected materials for 80 species of EN and ENA disjunct genera for transcriptome sequencing to investigate the pattern and rate of molecular evolution, and their relationships to morphological divergence and speciation. The study is in collaboration with colleagues at University of Florida and BGI in China. 3) Completed phylogenomic study of Forthergilla using GBS data. Manuscript was completed and accepted. Fothergilla (Hamamelidaceae) consists of F. gardenii (4x) from the coastal plains of the southeastern USA, F. major (6x) from the piedmont and mountains of the same region, and a few allopatric diploid populations of unknown taxonomic status. The study was to clarify relationships of the polyploid and diploid taxa. GBS data were generated for phylogeographic analyses of all 36 accessions of Fothergilla found in the wild. Sanger sequencing of three plastid and one nuclear regions were also conducted to provide data for comparison with GBS-based results. Results supported a genetically distinct 6x F. major and two lineages of the diploid populations closely associated with the 4x F. gardenii. The genetic structure suggested that the 4x F. gardenii originated through hybridization between the Gulf coastal 2x and an extinct (or undiscovered) 2x lineage, followed by backcrosses to the Atlantic coastal 2x before chromosome doubling, and the 6x F. major also originated from the "extinct" 2x lineage. Alternative scenarios were possible but are not as well supported.

Publications

• Type: Book Chapters Status: Accepted Year Published: 2015 Citation: 1. Xiang, QY(J). Aucubaceae. In: The Families and Genera of Vascular Plants (ed. K.Kubitzki). Vol. X. Asteridea (vol. Ed. J. W. Kadereit). In press. 2. Xiang, QY(J). Helwingiaceae. In: The Families and Genera of Vascular Plants (ed. K.Kubitzki). Vol. X. Asteridea (vol. Ed. J. W. Kadereit). In press. 3. GR.Plunkett, QY(J) Xiang, G Schutzs. Toricelliaceae. In: The Families and Genera of Vascular Plants (ed. K.Kubitzki). Vol. X. Asteridea (vol. Ed. J. W. Kadereit). In press.
• Type: Journal Articles Status: Published Year Published: 2015 Citation: 5. Call*, A, YX Sun*, Y Yu*, P Pearman, R Trigiano, DT Thomas, I Carbon, and QY(J) Xiang#. 2015. In revision. Population structure and Pleistocene biogeography of Cornus florida L. (Cornaceae) - integrating phylogeography and ecological niche modeling. Journal of Systematics and Evolution. DOI: 10.1111/jse.12171. 6. Qi*, ZC, Y Yu*, X Liu*, A Pais*, T Ranney#, R Whetten#, and Q-Y (J) Xiang#. 2015. Phylogenomics of polyploidy Fothergilla (Hamamelidaceae) by RAD-tag based GBSInsights into species origin and effects of software pipelines. Journal of Systematics and Evolution. DOI: 10.1111/jse.12176.
• Type: Journal Articles Status: Under Review Year Published: 2015 Citation: 3. Geng, XM, X Liu, M Ji, WH, A Grunden* and QY (J) Xiang*. 2016.. Enhancing heat tolerance of the little dogwood Cornus canadensis L. f. with introduction of a superoxide reductase gene from the hyperthermophilic archaeon Pyrococcus furiosus. Frontiers in Plant Sciences. Vol 6, article 26;| http://dx.doi.org/10.3389/fpls.2016.00026. 4. Liu, X, J Zhang, A Abuahmad, RG Franks*, D-Y Xie*, QY(J) Xiang*. 2016. Analysis of TFL1 homologs in dogwood species (Cornus L.) indicates functional conservation in control of transition to flowering. Planta.DOI :10.1007/s00425-016-2466-x.
• Type: Journal Articles Status: Under Review Year Published: 2015 Citation: 1. Ma, Q, X Liu, RG Franks*, QY(J) Xiang*. In Review. Alterations of CorTFL1 and CorAP1 expression correlate with major evolutionary shifts of inflorescence architecture in Cornus L. (Cornaceae)  a model for variation of determinate inflorescences. New Phytologist. Revision. 2. Yu4, Y*, QY(J) Xiang*, P Manos, DE Soltis, PS Soltis, BH Song, SF Chen, X Liu, G Wong. To be resubmitted next week. Whole genome duplication and acceleration of molecular evolution is associated with the early diversification of the genus Cornus L. (Cornaceae): Insights from De Novo Assembled Transcriptome Sequences. Molecular Biology and Evolution. In review
• Type: Conference Papers and Presentations Status: Other Year Published: 2015 Citation: 1. 2015. Dogwoods as a model for evo-devo genetic study of inflorescence morphology - tools and progresses. EDEN (Evolutionary Development and Ecology Network) Symposium, 2015 SDB 74th Annual Meeting, Salt Lake City, July. 2. 2014. Integrating Phylogeography, Ecological Niche Modeling, and Population Genomics For Biodiversity Conservation  A Case with the Flowering Dogwood Tree Under Fungal Pathogen Stress. State Key Lab for Biological Control, Sun Yat-Sen University, Guangzhou, China. 3. 2014. Fishing for candidate genes regulating inflorescence evolution in Cornus L. via de novo comparative transcriptome sequencing. The 109th West Lake Academic Forum of Zhejiang University --- Development and Trend of Plant Systematics and Evolution.

Progress 12/09/13 to 09/30/14

Outputs
Target Audience: undergraduate students, graduate students, and professional researchers and teachers in plant sciences and evoloutionary biology Changes/Problems: More geared toward genomics approach with next generation sequencing technology for high-throughput data that are more robust for the research. What opportunities for training and professional development has the project provided? Two Ph.D. students at NCSU, two visiting Ph.D. students co-trained with China, two visiting scientists from China, one undergraduate student at NCSU, one research specialist/technician. How have the results been disseminated to communities of interest? Publications of artciles in peer-reviewed journals in plant sciences and evolutionary biology; Presentation of research results at professional society conferences (Botanical Society of America, American Society of Plant Taxonomists, etc.) Invited Seminars What do you plan to do during the next reporting period to accomplish the goals? Begin to conducting comparative phylogenomic studies for tree genera and forest communities discontinously distributed in eastern Asia and eastern North America to understand factors shaping the assembly of biodiversity in these forests - new project Continue the population genomic study of Cornus florida and begin the genome sequencing project of the species with collaborators at other institutes with goals to identify genetic basis of disease resistance and local adaptation and unravel the evolutionary machanisms shaping the genetic structure of the species. Continue the evolutionary study of Cornales - using genome wide molecular data to reconstruct the phpylogeny and understand genome evolution. Continue the genetic study of dogwood flowering - identify genes controlling the inflorescence development and variation among species and evaluate gene functions via genetic transformation experiments.

Impacts
What was accomplished under these goals? see publicaitons

Publications

• Type: Journal Articles Status: Published Year Published: 2014 Citation: Kang, M, J Tao, J Wang, Q Qi, QY(J) Xiang, HW Huang. 2014. Adaptive and non-adaptive genome size evolution in Karst endemic flora of China. New Phytologist. DOI: 10.1111/nph.12726.
• Type: Journal Articles Status: Published Year Published: 2014 Citation: Wall, WA, N Douglas*, WA Hoffmann, TR Wentworth, JB Gray, QY(J) Xiang, BK Knaus and MG Hohmann. 2014. Evidence of population bottleneck in Astragalus michauxii (Fabaceae), a Fall-line Sandhills plant endemic to the southeastern United States. Conservation Genetics.15:153164. DOI 10.1007/s10592-013-0527-2.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Zhang*, J, RG Franks, X Liu*, M Kang, JEM Keebler, JE Schaff, HW Huang#, QY(J) Xiang#.2013. Comparative 454 transcriptome sequencing of dogwood inflorescences  characterization and identification of candidate genes for evolutionary developmental biology and phylogenomic studies. PLOS One. DOI: 10.1371/journal.pone.0082674
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Liu*, J, RG. Franks, CM Feng*, X Liu*, CX Fu, Q-Y(J) Xiang. 2013. Characterization of the sequence and expression pattern of LFY homologs from dogwoods species (Cornus L.) with divergent inflorescence architectures. Annals of Botany. Annals of Botany doi: 10.1093/aob/mct202.
• Type: Book Chapters Status: Published Year Published: 2013 Citation: Xiang, QY(J). 2013. Cornales (Dogwood). V2, a0024667. In eLS 2013, John Wiley & Sons Ltd: Chichester http://www.els.net/ [DOI: 10.1002/9780470015902.a0003729.pub2]
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Guo*, YL, A Pais*, AS. Weakley, QY (J) Xiang. 2013. Molecular Phylogenetic analysis suggests paraphyly and early diversification of Philadelphus (Hydrangeaceae) in western North America: New insights into affinity with Carpenteria. Journla of Systematics and Evolution. 51 (5): 545563. doi: 10.1111/jse.12041.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Zhao, YP*, WW Ma, QY Dai, ZC Qi, P Li. KM Cameron, J Lee, QY(J) Xiang#, CX Fu#. 2013. Comparative phylogeography of the Smilax hispida group (Smilacaceae) in eastern Asia and North America  implications in allopatric speciation, causes of diversity disparity, and origins of temperate elements in Mexico. Molecular Phylogenetics and Evolution. 68: 300311.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: 9. Liu*, X, CM Feng*, R Franks, R Qu, DY Xie, and QY(J) Xiang. 2013. Plant regeneration and genetic transformation of C. canadensis: a non-model plant appropriate for investigation of flower development in Cornus (Cornaceae). Plant Cell Report. 32: 77-87. Oneline first: 2012, DOI 10.1007/s00299-012-1341-x.