Plant DNA Barcodes: Applications Today and in The Future: Review

Journal of Systematics
JSE and Evolution doi: 10.1111/jse.12254
Review
Plant DNA barcodes: Applications today and in the future

W. John Kress*
Department of Botany, National Museum of Natural History, MRC-166, Smithsonian Institution, Washington, DC 20560, USA
*Author for correspondence. E-mail: KRESSJ@si.edu
Received 3 March 2017; Accepted 5 May 2017; Article first published online xx Month 2017
Abstract DNA barcodes have provided a new biological tool for organismal biologists to increase their
understanding of the natural world. Over the last decade four plant DNA barcode markers, rbcL, matK, trnH-
psbA, and ITS2, have been developed, tested, and used to address basic questions in systematics, ecology,
evolutionary biology and conservation, including community assembly, species interaction networks,
taxonomic discovery, and assessing priority areas for environmental protection. Forensic investigators have
also applied these plant DNA barcodes in the regulatory areas of traffic in endangered species and monitoring
commercial products, such as foods and herbal supplements. Major challenges ahead will focus on building the
global plant DNA barcode library and adopting genomic sequencing technologies for a more efficient and cost-
effective workflow in applying these genetic identification markers to additional fields of biological and
commercial endeavors.
Key words: conservation, DNA barcode library, forensics, forest dynamics plots, functional traits, genomics, identification,
metabarcoding, next-generation sequencing, phylogeny.
1 Introduction matK, trnH-psbA, and ITS) have generally been agreed upon as
the standard DNA barcodes of choice in most applications for
A major task for any plant systematist, field ecologist, plants (CBOL Plant Working Group, 2009; China Plant BOL
evolutionary biologist, conservationist, or applied forensic Group, 2011; Li et al., 2015).
specialist is to determine the correct identification of a plant The primary use of DNA barcodes is for species
sample in a rapid, repeatable, and reliable fashion. “DNA identification across the tree of life (Kress & Erickson,
barcodes,” i.e., standardized short sequences of DNA between 2012). By expanding the ability to diagnose a species of
400 and 800 base pairs long that in theory can be easily isolated plant during all stages of its life history (i.e., fruits, seeds,
and characterized for all species of plant on the planet, were seedlings, mature individuals both fertile and sterile) as well
originally conceived to facilitate this task (Hebert et al., 2003). as in damaged specimens, and in gut contents and in fecal
By combining the strengths of molecular genetics, sequencing samples of animals, DNA barcoding has become a universal
technologies, and bioinformatics, DNA barcodes offer a quick means of identification. The potential also exists to quantify
and accurate means to recognize previously known, described, the consistency of species definitions across lineages of
and named species and to retrieving information about them. plants with a measure of genetic variability based on the
This tool also has the potential to speed the discovery of the DNA barcode sequence data. As a biodiversity discovery
thousands of plant species yet to be named, especially in tool, DNA barcoding helps to flag species that are
tropical biomes (Cowan et al., 2006). potentially new to science, especially cryptic species (e.g.,
Hebert et al., 2004a). For the applied users of taxonomy,
DNA barcoding serves as a means to identify regulated
2 The Beginnings of Plant DNA Barcoding species, invasive species, and endangered species, and to
DNA barcodes as universally recoverable segments of DNA for test the identity and purity of botanical products, such as
the identification of species was initially designed and applied commercial herbal medicines and dietary supplements. DNA
for animals in the early years of the present century (Hebert barcodes are now also being used to address ecological,
et al., 2004b). In contrast a standard DNA barcode for plants evolutionary, and conservation issues, such as the ecologi-
was not immediately successful nor accepted by the botanical cal rules controlling the assembly of species in plant
community until several years later (see Kress, 2011). After an communities (e.g., Kress et al., 2009), the degree of
extensive inventory of gene regions in the mitochondrial, ecological specialization found in plant-animal networks
plastid, and nuclear genomes (e.g., Chase et al., 2005; Kress (e.g., Jurado-Rivera et al., 2009), and determining the most
et al., 2005; Kress & Erickson, 2007; Lahaye et al., 2008; evolutionarily diverse habitats for protection (Shapcott
Newmaster et al., 2008), four primary gene regions (rbcL, et al., 2015).
XXX 2017 | Volume 9999 | Issue 9999 | 1–17 © 2017 This article is a U.S. Government work and is in the public domain in the USA.
2 Kress
Fig. 1. Workflow indicating steps involved in plant DNA barcoding. In this example trees are sampled in a tropical forest inventory
plot. The workflow starts with tissue samples and vouchered herbarium specimens, and proceeds through generating DNA
barcode sequences to build the barcode library for use in taxonomic identification, species discovery, and ecological applications.
(from Kress et al., 2012).
The process of generating and applying plant DNA barcodes specimens. These vouchers serve as a critical permanent record
for the purpose of identification entails two basic steps: that connects the DNA barcode to a particular species of plant.
1) building the DNA barcode library of known species, and Once the DNA barcode library is complete for the organisms
2) matching the DNA barcode sequence of an unknown sample under study, whether they comprise a geographic region, a
against the DNA barcode library (Fig. 1). The first step requires taxonomic group, or a target assemblage (e.g., medicinal
taxonomists to select one to several individuals per species to plants, timber trees, etc.), then the DNA barcodes generated
serve as reference samples in the DNA barcode library. Tissue for the unidentified samples are compared to the known DNA
can be obtained from specimens already housed in herbaria barcodes using some type of matching algorithm.
or can be taken directly from live specimens in the field Since its initiation in 2003 DNA barcoding as a locus-based
with appropriately pressed, labeled, and mounted voucher endeavor developed in concert with genomics-based
J. Syst. Evol. 9999 (9999): 1–17, 2017 www.jse.ac.cn

Plant DNA barcode applications 3
investigations (Kress & Erickson, 2008a). DNA barcoding and and evolutionary relationships, and ecologists, who investigate
the field of genomics both share an emphasis on the species interactions and patterns of associations (Baker et al.,
acquisition of large-scale genetic data that offer new answers 2017). Plant DNA barcoding has been a boon to community
to questions previously beyond the reach of more data-limited ecologists seeking to understand the factors, such as species
disciplines. DNA barcodes aim to utilize the information in one diversity pools and functional traits, which control the assembly
or a few gene regions to discriminate among all species of life of species into ecological communities (Swenson, 2012).
whereas genomics, the inverse of DNA barcoding, describes in Estimating the third component controlling species assembly,
a fewer number of species the function and interactions namely evolutionary history, has always been hampered by the
across many if not all genes. It is expected that eventually, lack of well-resolved phylogenetic hypotheses on species
probably sooner than later, these ends of the genetic relationships in communities: Is there an underlying phyloge-
spectrum will merge together in methodologies and applica- netic structure among species in a community? Do closely
tions (Li et al., 2015; Coissac et al., 2016). related species prefer similar habitats and co-occur more or less
Over the last decade, the application of plant DNA barcodes frequently than expected at random? Phylomatic (Webb &
has accelerated, especially in the fields of ecology, evolution, Donoghue, 2005), a tool for estimating phylogenetic trees for
and conservation. Here I review some of the major break- plant communities, was a giant step forward for ecologists.
throughs and advances in using plant DNA barcodes to However, the publication of the first community phylogeny
investigate specific biological questions. I then conclude with based on DNA barcode sequence data for the trees in the forest
the prospects for building a global plant DNA barcode library dynamics plot on Barro Colorado Island in Panama (Kress et al.,
and applying new markers and sequencing technologies to 2009; Fig. 2) set off a storm of new investigations that were able
construct a better tool for botanical research. to add a well-supported evolutionary component to under-
standing species diversity and assembly (e.g., Gonzalez et al.,
2010; Kress et al., 2010; Pei et al., 2011; Swenson et al., 2012a;
3 Hotspots in the Application of Plant Whitfeld et al., 2012; Kaye M, unpublished data).
Determining if species in a community are more closely
DNA Barcodes Today related than by chance (phylogenetic clustering), more
It took nearly five years from the time of publication of the first distantly related than by chance (phylogenetic overdisper-
papers suggesting candidates for plant DNA barcode markers sion), or randomly distributed across the plant tree of life
(e.g., Kress et al., 2005) for the botanical community to reach can now be ascertained by building a DNA barcode library of
some consensus on the regions that showed the highest these species assemblages and generating a phylogenetic
promise of success (Lahaye et al, 2008; CBOL Plant Working tree based on the sequence data. The assumption follows
Group, 2009; Chen et al., 2010; China Plant BOL Group, 2011; that species in a community that are phylogenetically
Hollingsworth, 2011). It is still not uncommon to see clustered are more likely to have similar ecological niches
publications testing various markers in specific group of plants (i.e., phylogenetic niche conservation) and have been
(Wang et al., 2017). Yet, even before universal plant markers assembled via abiotic filtering. The contrasting assumption
were accepted systematists, ecologists, evolutionary biolo- is that phylogenetic overdispersion in a community is the
gists, and conservationists were already speculating and result of biotic interactions among sympatric species. Based
providing initial tests of the application of plant DNA barcodes on these assumptions the impact of evolutionary history on
to address critical questions in organismal biology (e.g., Kress & community structure has been investigated across stages of
Erickson, 2008b; Valentini et al, 2009). In the last five years, the forest succession (Whitfeld et al., 2012), among habitats
use of plant DNA barcodes has skyrocketed with several within a forest type (Oliveira et al., 2014), among forests
reviews of these applications already published (e.g., Hollings- across habitat gradients (Swenson et al., 2012a; Mi et al.,
worth et al., 2011; Erickson & Kress, 2012; Pecnikar & Buzan, 2012), and among communities across an entire country
2013; Joly et al., 2014; Kress et al., 2014). Categories of use (Muscarella et al., 2014) or across the globe (Erickson et al.,
include species level taxonomy, biodiversity inventories, 2014; Wills et al., 2016). Suddenly ecologists are evolutionary
phylogenetic evaluation, biosecurity and public health, conser- biologists!
vation assessment and environmental preservation, species The conclusions of these multiple studies in forest
interactions and ecological networks, cryptic diversity informa- communities based on DNA barcode phylogenies have
tion, DNA barcoding metadata, ecological forensics, commu- been varied. Phylogenetic signal can suggest the dominance
nity assembly, traffic in endangered species, and monitoring of of abiotic filtering in a particular forest habitat (Kaye M,
commercial products. In some cases, the methodologies are unpublished data) or it can vary across micro-habitats within
now advanced, while others remain in their infancy. a given forest (Kress et al., 2009; Pei et al., 2011), during
In this section the many uses of plant DNA barcodes will be succession (Whitfeld et al., 2012), or across forests at the
summarized in the broad areas of ecology, evolution, and landscape level (Muscarella et al., 2014) depending primarily
conservation, with a special emphasis on community phylog- on environmental factors (Muscarella et al., 2016). The
eny, functional traits and species assembly, species inter- generation of community phylogenies using DNA barcode
actions, species boundaries and discovery, DNA barcode data across multiple plots in varied habitats and environ-
forensics, and conservation. ments has great promise for further testing the basic
assumptions and rules governing species assemblies in plant
3.1 Community phylogeny and species assembly communities (see Erickson et al., 2014). And it is clear
DNA barcodes, as a tool, has greatly expanded the collabora- that this approach has yet to reach its full potential
tion between systematists, who focus on species identification (Swenson, 2013).
www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–17, 2017

4 Kress
Fig. 2. A community phylogeny constructed with plant DNA barcode sequence data. Maximum parsimony tree of 281 species of
woody plants in the Forest Dynamics Plot on Barro Colorado Island based on a supermatrix analysis of rbcL, matK, and trnH-psbA
sequence data. Color highlights indicate orders represented on BCI. The small tree at the bottom of the central column shows
just the ordinal relationships among the species in the BCI flora. (from Kress et al., 2009).

3.2 Functional traits and species assembly tropical landscapes in Costa Rica. Taken together these
As described above for investigations of community phyloge- investigations suggest, as concluded by Swenson (2013), that
netic histories, ecologists have long been interested in phylogenetic indictors are not always tied to ecological
quantifying critical plant traits that allow species to function determinants of community assembly. However, Swenson
in specific environments, and hence assemble into communi- also noted that both phylogenetic- and trait-based ap-
ties. Measuring the degree of similarity of traits in an proaches have greatly enhanced the understanding of
assemblage provides insights into those features that allow community assembly and their potential remains significant.
these species to coexist or not. Quantitative information on
functional traits together with well-resolved evolutionary 3.3 Species interactions: Identifying unknown partners
histories give ecologists a powerful tool for understanding the In order to fully understand the ecology and evolution of
processes of community assembly (Swenson, 2012). interactions among species in natural and human-altered
DNA barcodes alone do not provide specific new insights environments, accurate and repeatable identifications of the
into the role of functional traits in determining plant species interacting partners are imperative. Generalized interactions
assemblages. However, the DNA sequence data provide can be studied to some degree without clear identifications at
sufficient signal to derive phylogenetic hypotheses on the role the species-level of the organisms involved, i.e., only
of evolutionary signal in assembling species. It was hoped that identifying to genus or family. Specialized interactions,
the relationship of traits and phylogeny would allow the latter including mutualisms and antagonisms, require unambiguous
to be a strong predictor in measuring trait similarity across species identifications. The development of DNA barcodes as
species. Unfortunately the relationship between phylogeny species-level markers has already begun to revolutionize our
and functional traits is not always a direct correlation thereby understanding of species interactions and the community
preventing phylogenetic signal from being a proxy for networks they form, especially in tropical habitats where the
ecological similarity (Swenson et al., 2012b; Swenson, 2013). most complex interactions have evolved.
Nonetheless, since the publication of the first DNA barcode- One of the earliest applications of plant DNA barcodes to
based community phylogeny of tree species (Kress et al., investigate species interactions was employed almost simul-
2009), a host of investigations have combined data from taneously in both temperate and tropical ecosystems. The
functional traits with community phylogenies that together belowground interactions of plants in a community with each
have allowed ecologists to explore the processes determining other and with microbial communities in soils has been
community assembly in temperate, subtropical, and tropical exceptionally problematic to investigate because of difficulty
forests. In one of the largest investigations in tropical forests, in the identification of plant roots based on morphology
Baraloto et al. (2012) measured and compared 17 functional alone. However, once a DNA barcode library is developed for a
traits in 668 species across nine forest plots in the northern community based on the presence of aboveground repre-
Amazon region. Using two DNA barcode markers (rbcL and sentatives, species-specific genetic identification of the
matK) they found that functional trait similarity was greater belowground roots is facilitated. Kesanakurti et al. (2011)
than phylogenetic similarity in co-occurring species, and that investigated the spatial distribution of root diversity after a
both factors were significant in determining niche overlap. DNA barcode library was developed for the flora of an old-field
They concluded that environmental filtering had the strongest community in southern Ontario, Canada. Using the single DNA
impact on determining how tree species are assembled in barcode marker rbcL, they were able to correctly identify 85%
these tropical communities. Uriarte et al. (2010) reached of the root fragments that they sampled in 1 m deep soil
similar conclusions in an earlier study of eight traits measured profiles and found that the belowground diversity was more
across a small cohort of 19 tree species in a forest plot in highly structured ecologically than the aboveground diversity.
Puerto Rico. Using a DNA barcode-based community phylog- With respect to community assembly of these species in this
eny they found that at least three traits had significant impact old-filed habitat, both environmental filtering and competitive
on neighborhood structure even though a somewhat weaker interactions were determinants of below ground plant
phylogenetic signal was also present. Environmental filtering distributions.
was concluded to be the major force structuring this In a similar investigation in a more floristically diverse
community of trees. lowland tropical forest on Barro Colorado Island in Panama
The DNA barcode phylogeny generated for the approxi- (Jones et al., 2011), the belowground distribution of all trees
mately 300 species of trees on Barro Colorado Island in and lianas greater than 1 cm diameter were mapped using a
Panama has served as a template for a number of DNA barcode library already assembled for that flora (Kress
investigations of functional traits. The presence of evolution- et al., 2009). In this study the DNA barcode marker trnH-psbA
ary signal in such characteristics as soil associations (Schreeg proved to be quite effective in identifying both fine and small
et al., 2010), leaf toughness (Westbrook et al., 2011), wood coarse roots taken from 12 soil cores spread across a single
nitrogen concentration and life-history strategies (Martin hectare of forest. The underground species distributions were
et al., 2014), foliar spectral traits (McManus et al., 2016), and then compared with the aboveground distributions of
anti-herbivore defense traits (McManus et al., unpublished species. In general species interactions and spatial overlap
data) have all utilized the evolutionary information contained was greater belowground than expected based on above-
in the BCI community phylogeny. In general the patterns of ground stem densities (Fig. 3). Although this study raised
evolutionary signal varied in each of these functional traits several questions about methodology and analysis, it
across the tree species in the BCI plot. Lasky et al. (2014) also concluded that the potential for using DNA barcodes was
concluded that the association between evolutionary diversity high, which was similar to the conclusion reached in the
and functional diversity changed through forest succession in temperate old-field study (Kesanakurti et al., 2011). Both

6 Kress
Fig. 3. The distribution of underground roots as determined by plant DNA barcodes. Map from Barro Colorado Island in Panama
of the projected distribution of roots of four species in the top 20 cm of soil. The root sampling points at which roots of the focal
species were found are indicated with stars, with size scaled to the frequency of the species in proportion mass of samples
genotyped. The root sampling points at which no roots of the focal species were found are indicated by open diamonds. The
color shows the expected root density of the focal species under a best-fit model, with red indicating the highest value, yellow
intermediate, and white lowest. (from Jones et al., 2011).
studies also recognized that the application of next-genera- molecular markers and were only able to identity the hosts at
tion sequencing technologies and metabarcoding will be the generic or familial level.
required to streamline future studies of underground plant The most comprehensive analyses between herbivorous
interaction (e.g., Hiiesalu et al., 2012). beetles and their host plants have been conducted by Garcıa-
Food web interactions have been greatly clarified with the Robledo and colleagues. The host-specific relationships
application of DNA barcodes. Smith et al. (2011) using the CO1 between rolled-leaf beetles in the genera Cephaloleia and
DNA barcode marker were able to verify the food web Chelobasis (Chrysomelidae) and plants in the order Zingiber-
structure of the spruce budworm and its numerous para- ales have been well-studied, but the application of DNA
sitoids to understand the population dynamics of this major barcodes to both the beetles and the hosts have provided a
pest of trees in boreal forests. With regards to plant-herbivore much more detailed and quantitative measure of these
interactions, several teams of ecologists have been able to interactions (Garcıa-Robledo et al., 2013a; Fig. 4). One of
demonstrate the utility of DNA barcodes to identify the the advantages of using a multi-locus DNA barcode is that the
diversity of host plants for herbivorous beetles in both beetles can be identified to species at any of their life stages
neotropical (Jurado-Rivera et al., 2009; Pinzo n-Navarro et al., and not only as adults as in most previous investigations
2010) and Asian tropical forests (Kishimoto-Yamada et al., (Garcıa-Robledo et al., 2013b). Once the basic network of
2013). However, these studies used a limited number of foodweb interactions is established using DNA barcodes,

Fig. 4. A plant-herbivore network based on DNA barcodes. Reconstruction of a network using DNA extracted from beetle gut
contents. Rectangles represent insect herbivore and host plant species. Lines connect interacting species with colors
representing the taxonomic resolution at which each host plant association was identified. Host plant associations were inferred
from rbcL and ITS2 DNA fragments. Fragments were compared to host plant DNA barcode libraries containing sequences of all
potential hosts in the study area. Total species of insect ¼ 19; total species of plant ¼ 28; total number of interactions ¼ 74. (from
Garcıa-Robledo et al., 2013a).
comparisons can be made across habitats, elevations, and diets. Using DNA metabarcoding, they quantified diet
temperature gradients. It has been shown in numerous cases breadth, composition, and overlap for seven co-occurring
(e.g., Hebert et al., 2004a) that DNA barcodes can detect the species ranging in size from elephants to dik-diks. Conclusions
presence of cryptic species, especially in insects. This power of on competition and coexistence in these habitats based on
DNA barcoding has greatly improved the understanding earlier coarse-grained analyses were shown to be misleading
of species boundaries in the rolled-leaf beetles allowing for according to the more fine-grained taxonomic data provided
more precise mapping of the insect-host networks. The by the metabarcoding results. These same types of DNA
detection of these cryptic species clearly demonstrated that barcoding protocols have also been adapted to tracking and
the elevational distributions and thermal tolerances of the identifying the vectors of bird-dispersed fruits and seeds in the
beetles was much more narrow than previously thought, field (Gonzalez-Varo et al., 2014) in order to build a quantifiable
which will have an impact on the foodweb networks as network of frugivores and seed dispersal interactions.
climate change alters both host and herbivore migrations
(Garcıa-Robledo et al., 2016). 3.4 Species boundaries and biodiversity discovery
This detailed understanding of herbivore-host interactions Taxonomists have been using morphological features for the
using DNA barcodes has also been applied to large identification of both plants and animals since before the time
mammalian herbivores. Kartzinel et al. (2015) were able to of Carl von Linnaeus. Yet, even after hundreds of years of
determine the extent that sympatric mammalian browsers work by taxonomists perhaps only 20% of the species on earth
and grazers in a semiarid African savannah partitioned their have been formally recognized and named (Wilson, 2016).

8 Kress
Much work remains to be done. DNA barcoding provides a bioinformatics tools being used in different forest inventory
relatively new and significant tool to aid in the determination projects (e.g., RAINFOR [http://www.rainfor.org/], the
of species boundaries and discovery of new taxa. Janzen and Amazon Tree Diversity Network [ter Steege et al., 2013;
colleagues (e.g., Hebert et al., 2004a) have been pioneers in Fig. 5B], CForBio [http://www.cfbiodiv.org/], and ForestGEO
incorporating DNA barcode technologies for species discov- [Anderson-Teixeira et al., 2015]), will facilitate species
ery in the tropics, where the majority of biodiversity is found, discovery and taxonomic consistency across broad-scale
especially in certain insect groups. DNA barcoding is now a geographic zones (Dick & Webb, 2012). So far, such stand-
standard in their suite of tools being used for a broad-scale ardizations have not been fully adopted.
inventory of the caterpillars, their food plants, and their A recent example of how DNA barcodes could play a
parasitoids in Guanacaste, Costa Rica (Janzen et al., 2009). The decisive role in assisting taxonomic clarity is in the tree flora of
discovery and delimitation of cryptic species in other groups the Amazon Basin of South America. ter Steege et al. (2013)
of insects, such as beetles, is expanding our knowledge of assembled a massive data set on the distribution and
tropical diversity and species interactions (e.g., Garcıa- abundance of trees from forest inventory plots across
Robledo et al., 2013b, 2016; see above). Amazonia based on traditional taxonomic concepts and
Botanists have also applied DNA barcodes to species identifications and concluded that only 1.4% (227 species) of
inventories even though the discriminatory power of the the total estimated 16 000 tree species accounts for 50% of
barcode markers for plants is less than the barcode markers individual trees in the Amazon. These “hyperdominant”
for insects. Early studies (Gonzalez et al., 2009; Kress et al., species in general have wide distributions across the region.
2009; Dexter et al., 2010) mostly focused on trees in tropical The authors acknowledged that problems in their dataset
forest monitoring plots and demonstrated the difficulties, with taxonomic identification of trees are widespread and
especially the low identification rates (e.g., 70%), of using DNA lamented that the 5800 species of the rarest trees may never
barcodes. The same studies also pointed out the significant be properly identified, discovered, nor described because of
gains in being able to more accurately identify sterile and the lack of specimens with diagnostic flowers and fruits. DNA
juvenile specimens lacking traditional morphological features barcodes could provide a powerful tool to overcome these
required for identification. Costion et al. (2011) applied a three- hurdles. We generated DNA barcodes for several of these
locus DNA barcode (rbcL, matK, and trnH-psbA) to estimate hyperdominant species for which we had tissue samples from
tree species diversity in a taxonomically poorly known tropical across their ranges and found that some formed well-
rain forest plot in Queensland, Australia. They concluded that supported clusters of samples within a genus indicating
DNA barcodes were a significant aid in rapid biodiversity consistent identification by taxonomists. In other species
assessment and determination of cryptic tree populations, samples were not clustered within the genus suggesting that
even if they were not able to discriminate among all species in the outliers were either misidentified by taxonomists (often
the plot. A similar study in a central African rain forest plot from sterile specimens) or that the species as circumscribed is
using the same DNA barcode markers recognized the high not monophyletic and cryptic species may be present in these
discriminatory power at the genus-level (95%–100%), but plots (Kress WJ et al., unpublished data). Therefore, the
somewhat lower species-level success (71%–88%) in identifica- overall conclusions of ter Steege et al. (2013) on hyper-
tion, especially in species-rich clades. A DNA barcode library of dominance in the Amazonian tree flora may be in need of
the local species in these plots, including multiple accessions further study (see ter Steege et al., 2016). More widespread
of each species, greatly improved the successful identification application of DNA barcodes in taxonomic investigations of
at all taxonomic levels. tropical trees will provide more confidence in identifications
One of the major issues faced by plant taxonomists and and maybe even allow rapid discovery and description of
ecologists attempting to use DNA barcodes in hyper-diverse unknown taxa in these species-rich forests.
tropical forests is that many species are new to science,
therefore lack Latin binomials, and/or are members of poorly 3.5 DNA barcode forensics: Commercial products,
circumscribed species complexes that are difficult to identify endangered species, herbal supplements, and ethnobotany
even with traditional morphological data. Forest inventory The correct identification of plants and animals is equally
plots that have been set-up by ecologists to study forest important in the non-scientific, commercial world as it is to
dynamics of trees over time along elevational, latitudinal, or ecologists and taxonomists. Broadly termed “DNA barcode
habitat gradients are riddled with “morphotypes” lacking forensics,” genetic markers are being employed to insure
verified scientific names. Keeping track of these morphotypes commercial product identity and purity, to protect endan-
and comparing them among plots as well as comparing them gered species in illegal trading, and to document the use of
to known species is often difficult and prone to error (Gomes forest plants by local people. For example, the use of DNA
et al., 2013), but can be greatly enhanced by building DNA barcodes in determining species responsible for bird-strikes of
barcode libraries of these taxa (Dick & Webb, 2012; Fig. 5A). commercial aircraft is now routine (Dove et al., 2008). More
The critical role in species identification and discovery played widespread is the utilization of these markers in the
by herbarium voucher specimens, even if lacking flowers or authentication of animal and other wild-collected commercial
fruits, and the field data associated with these collections products sold in markets around the world (e.g., seafood:
cannot be overemphasized (Baker et al., 2017). Forest Nicole et al., 2012).
inventory plots in which trees are tagged for long-term The desire for an accurate, reliable, and inexpensive tool for
monitoring allow taxonomists to resample and collect the identification of illegal timber products has been one of
additional data from these individuals in the future if the driving forces in recent applications of DNA barcode
necessary. Standardizing the DNA barcode markers and technologies in several diverse regions of the world. Muellner

Fig. 5. Species discovery in forest dynamics and inventory plots. A, Summary of the workflow using plant DNA barcodes for
species discovery (adapted from Dick and Webb, 2012). B, A map of Amazonia showing the location of the 1430 Amazon Tree
Diversity Network plots. Orange circles indicate plots on terra firme; blue squares, plots on seasonally or permanently flooded
terrain; yellow triangles, plots on white-sand podzols; gray circles, plots only used for tree density calculations. CA, central
Amazonia; EA, eastern Amazonia; GS, Guyana Shield; SA, southern Amazonia; WAN, northern part of western Amazonia; WAS,
southern part of western Amazonia. (from ter Steege et al., 2013).
et al. (2011) tested a number of possible DNA barcode markers listed in the Convention on International Trade of Endangered
for the identification of species of trees in the commercially Species (CITES). A higher level of discrimination was
important mahogany family (Meliaceae). Although most demonstrated among commercially important, but threat-
markers fell short of expectations for discriminating species, ened species of trees of the tropical dry forests of India.
ITS was able to identify some species of this family that are Nithaniyal et al. (2014) used the standard plant DNA barcode

10 Kress
markers to accurately identify wood samples collected at constituent (Baker et al., 2012). In a follow-up to this study, a
timber processing plants in Andhra Pradesh and Tamil Nadu. comprehensive investigation of the authenticity of herbal
This same success was demonstrated in timber species found supplements and their contamination was conducted by
in Araucaria rain forests of the southern Atlantic coast of Brazil Newmaster et al. (2013). They build a well-documented DNA
(Bolson et al., 2015), which contains many threatened species barcode library (rbcL and ITS2) of the top 42 plant species used
of trees with high commercial importance, especially in the in the commercial trade in herbal supplements and then
family Lauraceae. Most recently, DNA barcoding was carefully analyzed the constituents in 44 herbal products
employed to monitor illegal timber trade in the biodiversity available on the market (Fig. 6). Their results, that 59% of the
hotspot of Madagascar, where species of Dalbergia (Faba- products contained plant species not listed on the labels
ceae), the rosewoods, are under threat. The limitations of the (many of them “fillers”), not only aroused attention in the
standard genetic markers in identifying closely related species scientific world, but made national news (see A. O’Connor,
was discouraging in this genus although some success was “Pills that aren’t what they seem,” New York Times, Tuesday 5
achieved (Hassold et al., 2016). Nonetheless regulators are in November 2013) and resulted in a backlash from the herbal
general optimistic that DNA barcode tools will be of assistance supplement community (Gafner et al., 2013). Newmaster et al.
in recognizing species currently protected by government (2013) concluded by recommending that the commercial
legislation, but under threat from illegal timber operations. In herbal industry should routinely use DNA barcoding as a
addition to timber trees, DNA barcode libraries have been verification of the authenticity of constituents in all herbal
developed for other taxonomic groups of threatened and products.
endangered taxa listed in CITES, e.g., orchids (Lahaye et al., One arena that is only now receiving sufficient attention is
2008) and it is expected that this technology will eventually the use of plant DNA barcodes in the documentation of
become standard in the monitoring of illegal trade. traditional ethnobotanical knowledge of Indigenous people. A
Timber is not the only commercial plant product in need of multifaceted project currently underway in the Sierra
accurate species identifications by regulators and quality Nororiental de Puebla, Mexico (Amith J & Kress WJ,
control specialists. Traditional medicines, teas, and herbal unpublished data) aims to combine local ethnobotanical
supplements together are an important and large component knowledge, linguistics, and cultural history, with DNA barcode
of the commercial market in biodiversity, locally, nationally, documentation of the regional flora to facilitate an under-
and internationally. It is estimated that medicinal plants standing of traditional ecological knowledge of the Nahuat
account for over US$60 billion in annual revenues in the and Totonac communities. Anthropologists and ethnobotan-
United States (see Newmaster et al., 2013, for a review of ists have been documenting such knowledge for centuries.
statistics on markets and use). From the early development of The inclusion of DNA barcoding technologies in this type of
plant DNA barcodes, applications to monitor this market have work allows the construction of a botanical reference library
been in development. Many of these investigations in which that will greatly facilitate the collection and accurate
DNA barcodes have been applied to commercial medicinals identification of the local flora and will demonstrate how
and herbal supplements have concluded that in some cases plants are named, classified, and used by Indigenous people.
the genetic markers used, which varied quite widely among
studies, were not able to discriminate among species. 3.6 Species and habitat conservation
However, more often the major obstacles were 1) the lack One of the major challenges facing biologists today is
of comprehensive DNA barcode libraries required to make conserving biodiversity under severe threat due to major
accurate comparisons of constituents of herbal teas and habitat degradation and environmental change caused by
supplements and 2) the lack of standardized, accurate humans. DNA barcoding, as a tool primarily for species
taxonomy and common names listed in the herbal literature,
catalogs, and pharmacopeias. Stoeckle et al. (2011) could not
identify many of the constituents in the herbal teas they
tested using the standard markers rbcL and matK, but more
problematic was the lack of comparable sequence data at that
time for many of the plants found in the commercial products.
The basic taxonomic problem of obsolete or dated nomen-
clature in the literature on traditional medicines, rather than
species discrimination, was a major hurdle in a study of the
local trade in medicinal roots in Northern Africa using plant
DNA barcoding (de Boer et al., 2014).
Even if herbal products may be pure and reliable as to
species identification when locally collected, the final
products used by consumers are often mislabeled or are
adulterated with additional plant species. In a seminal study of
the authenticity of herbal preparations in the United States, it
was demonstrated using DNA barcodes that substitutes for
black cohosh (Actaea racemosa; Ranunculaceae), a common Fig. 6. The application of DNA barcodes to test the purity of
herb used by post-menopausal women as a substitute for herbal supplements and medicinals. DNA barcode results from
hormone replacement therapy, were present in only nine of blind testing of the 44 herbal products representing 30
36 commercially available products that listed this species as a medicinal species of plants. (from Newmaster et al., 2013).

identification, can be used in two specific ways to address

biodiversity conservation: 1) as a means of more accurate and
eventually more rapid biodiversity monitoring both before
and after conservation actions, and 2) by providing data that
will assist in estimations of phylogenetic diversity for setting
conservation priorities (Krishnamurthy & Francis, 2012).
Making accurate taxonomic determinations for conserva-
tion monitoring can be greatly aided with plant DNA
barcodes, especially in tropical biomes where biodiversity is
poorly known and many species lack verified scientific
names. As pointed out above with respect to herbal
supplements and medicines, the deficiency of uniform
taxonomy is a significant problem in assessing species
diversity and identification in local market products. The
same applies to poorly known tropical forests requiring
conservation in which species identification is extremely
difficult, especially when using non-fertile specimens often
only labeled as “morphospecies” (Gomes et al., 2013). In
such cases DNA barcoding offers a solution for more
uniform identifications, although some logistical hurdles
may still impede the widespread use of DNA barcodes in this
fashion (Gonzalez et al., 2009).
With regard to determining conservation priorities, it has Fig. 7. Using DNA barcodes to map phylogenetic diversity for
been demonstrated that plant DNA barcodes can play a key habitat conservation. Graphical representation derived from
role in estimating species richness in the relatively poorly the phylogenetic tree for SE Queensland based on three DNA
known northern tropical forests of Queensland, Australia barcode markers indicating by colored bars the species
(Costion et al., 2011). More recently the fragmented rain forest present in each of the subregions. (from Shapcott et al., 2015).
habitats in South Eastern Queensland, whose distributions
and extent reflect both past climate change as well as recent
agricultural use, have received renewed conservation atten- by IUCN criteria, it is now suspected that this species is extinct
tion. These forests are taxonomically rich at the generic-level (Costion et al., 2016).
and less so at the species-level, so that species richness may DNA barcodes are only in their infancy as applications for
not be the most appropriate measure for setting conservation understanding and enhancing conservation efforts. However,
priorities. Shapcott et al. (2015, 2017) generated plant DNA published studies to date suggest that standardized and
barcodes (rbcL, matK, and trnH-psbA) for 770 species in 111 comparable genetic information for species across broad
families that accounted for 86% of the rain forest flora in South geographic regions, such as sequence data provided by DNA
Eastern Queensland and calculated phylogenetic diversity barcodes, are a powerful tool and can have a significant
(PD; see Faith, 2008) measures for each of the 18 subregions in impact on basic research (e.g., Mi et al., 2012; Erickson et al.,
the area (Fig. 7). They concluded that PD was correlated with 2014; Pei et al., 2015) as well as conservation monitoring and
species richness across the subregions and used these priority assessments in threatened habitats, in local commu-
estimates to prioritize subregions for conservation action. It nities and across large geographic regions (e.g., Shapcott
was also determined, using the phylogenetic measures et al., 2015).
provided by the DNA barcode sequence data, that the local
floristic patterns were consistent with both ancient ecological
refugia (phylogenetically overdispersed species) and recent 4 Tomorrow’s Outlook for Plant DNA
lineage range expansions (phylogenetically clustered species)
that explained the conservation priorities (Howard et al.,
Barcoding
2016). Since the time of their introduction into the botanical
Even though the earth may be undergoing its sixth major community over a decade ago DNA barcodes have been
extinction with extinction rates over 1000 times normal applied to a variety of investigations in both basic and applied
(Wilson, 2016), observing a species extinction event is rare. research in plants. One of the main reasons that plant
Plant DNA barcodes were used to verify that a narrow range systematists have not yet universally accepted DNA barcoding
endemic tree in the family Rubiaceae, known only from two as a core tool in their arsenal for identifying species is that no
mature individuals on the island of Palau in Micronesia, was single marker is able to completely discriminate among
most likely a distinct species in the genus Timonius (Costion species in most taxonomic groups. In contrast ecologists have
et al., 2016). Additional morphological and molecular data been more willing to find new and unique applications of DNA
verified that this taxon was T. salsedoi Fosberg & Sachet barcodes to address some of their basic research questions
described in the 1980s. In 2014 after a survey of the island because in general they work in systems made up of multiple
where these two individuals were known to occur it was lineages of plants that can be uniquely identified by a
discovered that both trees had succumbed when a typhoon combination of DNA barcode loci. Looking to the future, plant
hit the area. Previously recommended as Critically Endangered DNA barcoding will advance in two key ways to serve the

12 Kress
botanical community by: 1) building a more comprehensive build floristic DNA barcode libraries are being conducted
global plant DNA barcode library for universal use, and 2) usually at the state or regional level and primarily in the
developing new markers and adopting new sequencing temperate zone (e.g., Wisconsin, USA, Givnish T, pers.
technologies. comm.).
The biggest hurdle in this approach to populating the global
4.1 Building the global plant DNA barcode library DNA barcode library is identifying funding resources to cover
When the first well-supported community phylogeny was the sequencing and laboratory costs, which most often come
constructed using plant DNA barcodes for the 296 species of from government funding agencies. Increasing interest is
trees in the 50 hectare forest dynamics plot on Barro Colorado being shown by government bureaus that are responsible for
Island in Panama (Kress et al., 2009), a light bulb went off in regulating the transport of biological materials (e.g., the US
the minds of every community ecologist working in long-term Department of Agriculture) and crime investigation (e.g., the
forest monitoring plots around the world. Soon trees in plots US Federal Bureau of Investigation). Achieving the goal of
across the globe were being DNA barcoded from the providing a universal library of DNA barcodes for all species of
neotropics (Gonzalez et al., 2009; Kress et al., 2010) to Africa plants in the world is still far in the future, but once available,
(Parmentier et al., 2013) to Asia (Pei et al., 2011; Huang et al., both basic and applied research will benefit greatly.
2015). Eventually DNA barcode sequence data (rbcL, matK,
and trnH-psbA) were generated and compared across 15 4.2 New DNA markers and new sequencing technologies
forest plots in the CTFS/ForestGEO network representing 1347 Speculation and predictions on the future direction of plant
species of trees in both temperate and tropical habitats in DNA barcoding began almost simultaneously with the
seven different countries (Kress et al., 2012; Erickson et al., initiation of studies applying these markers to questions in
2014). DNA barcodes have also been generated for many taxonomy, evolution, and ecology, including the relationship
additional plots that are not part of this particular network. between locus-based DNA barcodes and genomic approaches
The CTFS/ForestGEO is emphasized here because it represents to species identification (Kress & Erickson, 2008a). The need
one of the largest network of long-term forest monitoring for both advanced sequencing technologies as well as
plots that is implementing DNA barcoding as a standard efficient database design and search strategies for species
protocol over more than 60 plots in 24 countries world-wide identification were recognized.
(Anderson-Teixeira et al., 2015). To date three-locus DNA One exciting modification of DNA barcoding is appropri-
barcodes have been generated for over 3000 species of plants ately called “metabarcoding” or “eDNA” (Taberlet et al.,
in 28 plots; a complete DNA barcode library for all plots will 2012), which employs genetic markers for the identification of
include over 10 000 species of trees and probably two to three organisms in environmental samples, such as soil, sea water,
times as many lianas, shrubs, and herbs. or coral reefs (Leray & Knowlton, 2015). Successful identifica-
Populating the global plant DNA barcode library is one of tion of organisms in these environments usually requires very
the biggest challenges for the next decade. These forest short and unique genetic markers (often not the standard
monitoring plots represent a rich resource for building the DNA barcode sequence regions) or “mini-barcodes,” which
plant DNA barcode library because in general they have well- use a sub-region of the standardized markers, for overcoming
verified identifications, vouchered collections, and individually the problem of degraded DNA in these samples (Hajibabaei &
tagged trees that can be re-visited by botanists if necessary. McKenna, 2012). The same techniques have also been applied
Two additional avenues for developing the library for plants to studies using ancient DNA (Willerslev et al., 2007).
include lineage-based efforts and floristic efforts. Individual However, it is also possible to use some of the standard
taxonomists are also generating DNA barcodes for specific plant DNA barcode markers (e.g., rbcL and ITS2) to determine
groups of plants as either trials for sequencing success using the composition of plant species in a community by analyzing
the standard markers (e.g., Chen et al., 2010, 2015; Wang et al., soil samples (Jones et al., 2011; Fahner et al., 2016). The field of
2017) or as part of their basic molecular phylogenetic metabarcoding is rapidly developing through improvements
investigations in which the DNA barcode markers are used in methodology, such as the recovery, amplifying, and
for understanding evolutionary relationships. Although many sequencing of short DNA fragments. In addition creating
of these “DNA barcodes” may not receive the official GenBank new bioinformatics tools for transforming a list of DNA
DNA barcode designation, they are all adding to the library of sequences present in a sample into a list of identifiable species
sequences that complement the standard DNA barcode is formidable, but will eventually be adequately addressed.
markers. The combination, complementation, and extension of
Recently major efforts have begun to generate DNA employing the standard single- or multi-locus DNA barcodes
barcodes for entire regional floras. One of the most with next generation sequencing (NGS) technologies has
impressive is the library that has been built for identifying been inevitable. The divide between specimen-based DNA
the vascular plants of Canada (Braukmann et al., 2017). barcoding and environment-based metabarcoding as de-
Braukmann and colleagues successfully generated barcode scribed above has been in part responsible for this turn to
sequence records for 96% of the 5108 species known from NGS. It has been suggested that genome skimming (i.e., low-
Canada. Each of the three markers they used (rbcL, matK, and coverage shotgun sequencing) of both plastid and nuclear
ITS2) varied in its success of coverage across the species pool. regions as an “extended DNA barcode” may serve as the
Their results indicated that these markers were highly bridge between standard DNA barcoding and whole genome
successful in identifying plants at the level of genus across sequences as the ultimate in species identification (Coissac
the region and demonstrated best species discrimination in et al., 2016; Hollingsworth et al., 2016; Fig. 8). Such “mega-
subregions of the highest floristic diversity. Other efforts to barcoding” will not only circumvent the need for PCR, but will

Fig. 8. Plant DNA barcoding moves towards genomics. Overview of the experimental procedures for implementing extended
DNA barcoding based on one gigabase of sequence reads produced by shotgun sequencing of genomic DNA. (adapted from
Coissac et al., 2016).
also provide an increased level of genetic data that can serve DNA barcoding at all as originally envisioned, as it offers a very
other purposes besides species identification (e.g., phyloge- idiosyncratic methodology and not a rapid and universal
netic resolution). approach for species identification.
However, for plants some researchers are also advocating a The implementation of other sequencing technologies,
focus on chloroplast genome sequencing as “super-barcodes” such as the utilization of microfluidic PCR-based target
to eventually replace the locus-based approach. Li et al. (2015) enrichment that may offer a faster and less expensive option
provide a thorough review of locus-based developments and for large-scale multi-locus plant DNA barcoding (Gostel M,
suggest a new approach to plant DNA barcoding that pers. comm.), are indicative of the current state of innovations
combines these super-barcodes with the design and selection in genomics. Many of these methodologies are still in their
of “specific-barcode” loci for individual species groups. They infancy and may yet prove to advance our ability to apply
term this as the “1 þ 1 Model” for plant DNA barcoding. genetic markers to fulfill the goals of DNA barcoding.
However, they also recognize that this method, even if it will However, as we seek new methods we must not lose sight
provide a reliable barcode for accurate plant identification, “is of the original purpose of DNA barcoding, namely species
not yet resource-effective and does not yet offer the speed of identification! In plants, as many have pointed out, universal
analysis provided by single locus barcodes to unspecialized species discrimination may never be possible with a locus-
laboratory facilities.” Indeed, their model may not be plant based approach; neither plastid data alone nor even with a

14 Kress
significant amount of information from the nuclear genome Baraloto C, Hardy OJ, Paine CET, Dexter KG, Cruaud C, Dunning LT,
will suffice. However, there will always be a tradeoff between Gonzalez M, Molino J, Sabatier D, Savolainen V, Chave J. 2012.
the ability to provide absolute universal species discrimination Using functional traits and phylogenetic trees to examine the
and the level of effort and cost to achieve that goal. As assembly of tropical tree communities. Journal of Ecology 100:
taxonomists, ecologists, and applied scientists we must ask 690–701.
ourselves if 70–90% species discrimination with standard DNA Bolson M, Smidt EC, Brotto ML, Silva-Pereira V. 2015. ITS and trnH-
barcoding methods is sufficient if the cost is only 10% of the psbA as efficient DNA barcodes to identify threatened commer-
cost of whole genome sequencing. Are the current technolo- cial woody angiosperms from Southern Brazilian Atlantic rain-
forests. PLoS ONE 10: e0143049.
gies adequate and appropriate for most goals envisioned for
DNA barcoding? Maybe they are. However, as technological Braukmann TWA, Kuzmina ML, Sills J, Zakharov EV, Hebert PDN. 2017.
advances rapidly decrease costs and increase efficiencies, Testing the efficacy of DNA barcodes for identifying the vascular
plants of Canada. PLoS ONE 12(1): e0169515. doi:10.1371/journal.
maybe they will not be. The near future will provide a quick
pone.0169515.
and final answer.
CBOL Plant Working Group. 2009. A DNA barcode for land plants.
Proceedings of the National Academy of Sciences USA 106:
12794–12797.
Acknowledgements Chase MW, Salamin N, Wilkinson M, Dunwell JM, Kesanakurthi RP,
I would like to thank the many co-authors, collaborators, post- Haider N, Savolainen V. 2005. Land plants and DNA barcodes:
docs, technicians, and interns who I have had the pleasure of Short-term and long-term goals. Philosophical Transactions of the
working with to advance the field of DNA barcoding. I am Royal Society B Biological Sciences 360: 1889–1895.
especially indebted to those colleagues who have provided Chen J, Zhao J, Erickson DL, Xia N, Kress WJ. 2015. Testing DNA barcodes
inspiration, encouragement, advice, and assistance along the in closely related species of Curcuma (Zingiberaceae) from
way, including Stuart Davies, Dave Erickson, Paul Hebert, Myanmar and China. Molecular Ecology Resources 15: 337–348.
Peter Hollingsworth, Dan Janzen, Kristen Lehman, De-Zhu Li, Chen S, Yao H, Han J, Liu C, Song J, Shi L, Zhu Y, Ma X, Gao T, Pang X,
Ida Lopez, Scott Miller, Nancai Pei, Carlos Garcıa-Robledo, Luo K, Li Y, Li X, Jia X, Lin Y, Leon C. 2010. Validation of the ITS2
David Schindel, Alison Shapcott, Nate Swenson, and Joe region as a novel DNA barcode for identifying medicinal plant
Wright. I have no conflicts of interest in the publication of this species. PLoS ONE 5: e8613.
work. China Plant BOL Group. 2011. Comparative analysis of a large dataset
indicates that internal transcribed spacer (ITS) should be
incorporated into the core barcode for seed plants. Proceedings
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Journal of Systematics

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Plant DNA barcodes: Applications today and in the future

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www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–17, 2017

J. Syst. Evol. 9999 (9999): 1–17, 2017 www.jse.ac.cn

www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–17, 2017

J. Syst. Evol. 9999 (9999): 1–17, 2017 www.jse.ac.cn

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J. Syst. Evol. 9999 (9999): 1–17, 2017 www.jse.ac.cn

www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–17, 2017

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identification, can be used in two specific ways to address

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