Phylogeny and Taxonomic Synopsis of the Genus Bougainvillea (Nyctaginaceae)

Bougainvillea Comm. ex Juss. is one of the renowned genera in the Nyctaginaceae, but despite its recognized horticultural value, the taxonomy and phylogeny of the genus is not well-studied. Phylogenetic reconstructions based on plastid genomes showed that B. pachyphylla and B. peruviana are basal taxa, while B. spinosa is sister to two distinct clades: the predominantly cultivated Bougainvillea clade (B. spectabilis, B. glabra, B. arborea, B. cultivar, B. praecox) and the clade containing wild species of Bougainvillea (B. berberidifolia, B. campanulata, B. infesta, B. modesta, B. luteoalba, B. stipitata, and B. stipitata var. grisebachiana). Early divergence of B. peruviana, B. pachyphylla and B. spinosa is highly supported, thus the previously proposed division of Bougainvillea into two subgenera (Bougainvillea and Tricycla) was not reflected in this study. Morphological analysis also revealed that leaf arrangement, size, and indumentum together with the perianth tube and anthocarp shape and indumentum are important characteristics in differentiating the species of Bougainvillea. In the present study, 11 species and one variety are recognized in Bougainvillea. Six names are newly reduced to synonymy, and lectotypes are designated for 27 names. In addition, a revised identification key and illustrations of the distinguishing parts are also provided in the paper.


Introduction
Bougainvillea Comm. ex Juss. (Nyctaginaceae; Bouginvilleeae) is a commonly cultivated plant group with colorful bracts in the four o'clock family. The type species, Bougainvillea spectabilis, was discovered by the French botanist Philibert Commerson (with his assistant Jean Baret) in Rio de Janeiro, Brazil, during the 1760s [1]. Commerson was the botanist accompanying French Navy Admiral Louis-Antoine de Bougainville on the voyage to circumnavigate the Earth. Since de Bougainville was the commander of the voyage, the newly discovered genus was named after him. The genus name, originally spelled Bugainvillaea Jussieu [2], has many orthographic variants. Spach [3] was the first to adopt the spelling Bougainvillea, which was later conserved [4,5] and listed in Appendix III of the International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) [6]. Most species of Bougainvillea were published by Heimerl [7], Standley [8][9][10], and Toursarkissian [11]. Based on previous publications, 14-18 species of Bougainvillea have been recognized, although the basis for separating the species and the differences between them may be inconsequential since they are highly similar in appearance [8]. We recognize 11 species here.
Morphologically, plants of Bougainvillea are scandent shrubs or small trees often armed with simple or forked thorns. The colorful structures often mistaken as flowers are actually modified bracts surrounding small tubular flowers. The flower is usually attached to the inner surface of each bract and its pedicel is confluent with the midrib of the bract [12]. Based mainly on the branching of the thorn apex, Standley [10] divided Bougainvillea into two subgenera: subg. Tricycla and subg. Eubougainvillea. According to Art. 21.3 and 22.2 of the Shenzhen Code [6], Eubougainvillea may be corrected to Bougainvillea. Only Bougainvillea spinosa with furcate or forked thorns was categorized into subg. Tricycla, while the remaining species were classified into subg. Bougainvillea. Bract size and color were considered important characters in subdividing Bougainvillea into two unnamed groups. The first group, with large (ca. 2.5 to 4 cm long), brightly colored bracts, contains B. pachyphylla, B. peruviana, B. glabra, and B. spectabilis. The second group, which has smaller (<2.5 cm long) and less conspicuous bracts or sometimes brightly colored bracts that do not retain their color as they dry, contains B. berberidifolia, B. campanulata, B. infesta, B. praecox, and B. stipitata [8,10]. This proposed subdivision was based entirely on morphological characteristics.
In previous phylogenetic studies of the Caryophyllales, Bougainvillea together with other genera in Nyctaginaceae was placed in the phytolaccoid clade of a larger 'globular inclusion' clade [13][14][15]. The molecular phylogeny of Nyctaginaceae [16] based on three plastid genes (ndhF, rps16, rpl16) and one nuclear region (nrITS) significantly developed the understanding of the relationships within the family, ensuing the reevaluation of the tribal classification [17]. Although Douglas and Manos [16] involved nearly all genera of Nyctaginaceae in their study, only partial sequences of Bougainvillea glabra and B. infesta were included. Douglas and Manos [16] fully resolved the position of Bougainvillea within Nyctaginaceae as sister to Belemia and Phaeoptilum, but the relationship among the species of Bougainvillea was not established in their paper. A recent study on the plastid genomes of some wild and cultivated plants of Bougainvillea showed that B. peruviana and B. pachyphylla diverged earlier than other species of Bougainvillea, while the commonly known B. glabra clustered with B. spectabilis and a B. cultivar [18]. Since only a few samples were included in the analysis, limited information about the relationship among the species of Bougainvillea was inferred. Thus, the current study reported here sought to describe the phylogenetic relationships within Bougainvillea and to provide a taxonomic synopsis of the genus.
Plants 2022, 11, 1700 3 of 20 content of each chloroplast genome was highly similar as well, ranging from 36.4% to 36.6%. . Genes within the circle were also color-coded according to their functional group. The dark gray and light gray plots correspond to the GC and AT contents, respectively.

SNPs and Indels Analysis
The SNPs (single nucleotide polymorphisms) and indels (insertions-deletions) were identified in the plastid genomes of Bougainvillea using MUMmer4 [19] and Geneious Prime 2020.1 [20]. The overall results indicated that there were more SNPs and indels in the chloroplast genomes of B. pachyphylla, B. peruviana, and B. modesta. This can be . Genes within the circle were also color-coded according to their functional group. The dark gray and light gray plots correspond to the GC and AT contents, respectively.

SNPs and Indels Analysis
The SNPs (single nucleotide polymorphisms) and indels (insertions-deletions) were identified in the plastid genomes of Bougainvillea using MUMmer4 [19] and Geneious Prime 2020.1 [20]. The overall results indicated that there were more SNPs and indels in the chloroplast genomes of B. pachyphylla, B. peruviana, and B. modesta. This can be attributed to the fact that the three aforementioned species were distantly related to the reference species, B. glabra. The non-coding sequences of B. pachphylla had 571 SNPs while the coding sequences had 317 SNPs. Correspondingly, there were 545 SNPs in the non-coding sequences and 337 SNPs in the coding sequences of B. modesta (Figure 2A). In contrast, B. praecox (309, 200), B. spectabilis (283, 195), B. cultivar (282, 163), and B. arborea (245, 135) had fewer SNPs, suggesting that those genomes are highly similar to the reference genome of B. glabra. In congruence with the preceding study [18], several protein-coding genes had a higher frequency of SNPs. The ycf 1 reading frame had the greatest number of synonymous and non-synonymous SNPs in all samples of Bougainvillea. (Figure 2B). In addition, the genes for RNA polymerase (rpoA, rpoB, rpoC2, rpoC1), NADH-dehydrogenase (ndhF, ndhA), rubisco (rbcL), maturase (matK), and hypothetical reading frames (ycf 1, ycf 2) contained relatively more synonymous and non-synonymous SNPs. The patterns of synonymous (Ks) and non-synonymous (Ka) substitutions also revealed that those genes are possibly under significant positive selection since they have Ka/Ks values > 1.
greatest number of synonymous and non-synonymous SNPs in all samples of Bougainvillea. (Figure 2B). In addition, the genes for RNA polymerase (rpoA, rpoB, rpoC2, rpoC1), NADH-dehydrogenase (ndhF, ndhA), rubisco (rbcL), maturase (matK), and hypothetical reading frames (ycf1, ycf2) contained relatively more synonymous and nonsynonymous SNPs. The patterns of synonymous (Ks) and non-synonymous (Ka) substitutions also revealed that those genes are possibly under significant positive selection since they have Ka/Ks values > 1.  Figure 3A). Bougainvillea arborea had the fewest indels, denoting fewer differences from the reference species, B. glabra. The presence of large indels (16-55 bp) in the clpP introns of almost all species mainly differentiated B. glabra from other species. Both B. peruviana and B. pachyphylla differed as well from B. glabra by the large deletion (43 bp) between the rpl22 and rps19 genes ( Figure S1). When compared to B. glabra, several deletions were observed in most wild species of Bougainvillea ( Figure S1). A 16-bp deletion was discovered in the rps16 introns of B. berberidifolia, B. campanulata, B. infesta, B. modesta, B. luteoalba, B. stipitata and B. stipitata var. grisebachiana. Additionally, deletions in the trnR-AGC-trnN-GUU (28 bp) and rpl32-trnL-UAG (36-42 bp) spacers were detected in the wild species of Bougainvillea ( Figure S1). Even though small indels are more common in the non-coding sequences, small deletions were found in the matK (6 bp) and accD (9 bp and 6 bp) genes of the wild species of Bougainvillea ( Figure S1). A large number of indels were also found in the ycf 1 genes of all cp genomes of Bougainvillea ( Figure 3B). deletions were observed in most wild species of Bougainvillea ( Figure S1). A 16-bp deletion was discovered in the rps16 introns of B. berberidifolia, B. campanulata, B. infesta, B. modesta, B. luteoalba, B. stipitata and B. stipitata var. grisebachiana. Additionally, deletions in the trnR-AGC-trnN-GUU (28 bp) and rpl32-trnL-UAG (36-42 bp) spacers were detected in the wild species of Bougainvillea ( Figure S1). Even though small indels are more common in the non-coding sequences, small deletions were found in the matK (6 bp) and accD (9 bp and 6 bp) genes of the wild species of Bougainvillea ( Figure S1). A large number of indels were also found in the ycf1 genes of all cp genomes of Bougainvillea ( Figure 3B).

Phylogenetic Analysis
Phylogenetic trees reconstructed with Bayesian Inference (BI) and Maximum Likelihood (ML) analyses resulted in congruent topologies and differed only in support

Discussion
The plastid-based phylogeny obtained in this analysis strongly supported the early divergence of both Bougainvillea peruviana and B. pachyphylla. Consistent with a prior study [18], these two are considered the basal-most species of Bougainvillea. In morphological features, B. peruviana was associated with either B. glabra [8,21] or B. pachyphylla [10], but genetic information from plastid genomes confirmed a higher affinity with B. pachyphylla [18]. The analyses of SNPs and indels presented in this study also signified that B. peruvi- In the predominantly cultivated Bougainvillea group (clade II), the inconspicuous Bougainvillea praecox was sister to two apparent subclades containing B. glabra and B. spectabilis (BS = 100, BPP = 1) (Figure 4). Within the 'glabra' subclade, B. arborea samples were grouped together with B. glabra (BS = 100, BPP = 1). In contrast, the Bougainvillea cultivar representative was clustered with B. spectabilis (BS = 100, BPP = 1). Clade III, composed mainly of wild species, displayed no specific grouping pattern. Bougainvillea stipitata was in the basal position, a grade higher than the remaining wild species of Bougainvillea. Bougainvillea berberidifolia, B. campanulata, B. infesta, and B. modesta subsequently followed B. stipitata. Bougainvillea modesta had a closer relationship to B. infesta than with the rest of Bougainvillea (BS = 100, BPP = 1).

Discussion
The plastid-based phylogeny obtained in this analysis strongly supported the early divergence of both Bougainvillea peruviana and B. pachyphylla. Consistent with a prior study [18], these two are considered the basal-most species of Bougainvillea. In morphologi-Plants 2022, 11, 1700 7 of 20 cal features, B. peruviana was associated with either B. glabra [8,21] or B. pachyphylla [10], but genetic information from plastid genomes confirmed a higher affinity with B. pachyphylla [18]. The analyses of SNPs and indels presented in this study also signified that B. peruviana and B. pachyphylla represented two genomes distinct from B. glabra. Both species are morphologically similar except in leaf texture and perianth indumentum. Bougainvillea peruviana has a thin leaf blade and a glabrous perianth in contrast to the thick leathery leaf blade and densely puberulent perianth of B. pachyphylla [9,10]. Both B. peruviana and B. pachyphylla have a slender, almost linear-oblong perianth tube but the tube of the latter is a bit wider near the perianth lobes ( Figure 5). Early divergence of these two taxa also suggests that the two subgenera (Tricycla and Bougainvillea) classification of Standley [10] does not coincide with the current analysis. Bougainvillea pachyphylla and B. peruviana are not closely related to other members of subg. Bougainvillea. Though B. pachyphylla and B. peruviana have simple thorns similar to the other species of Bougainvillea, they are more basal than B. spinosa (subg. Tricycla), suggesting that the Bougainvillea cannot be subdivided based on thorn branching alone.  Bougainvillea spinosa differs from other species of Bougainvillea by having forked or furcate thorns [8]. Moreover, the solitary flower surrounded by three bracts and the thick, fleshy leaves arranged into brachyblasts makes it more morphologically distinct from other species. Consequently, earlier classifications treated B. spinosa as a single species of subgenus Tricycla. The molecular analysis did not concur with this classification, but it Bougainvillea spinosa differs from other species of Bougainvillea by having forked or furcate thorns [8]. Moreover, the solitary flower surrounded by three bracts and the thick, fleshy leaves arranged into brachyblasts makes it more morphologically distinct from other species. Consequently, earlier classifications treated B. spinosa as a single species of subgenus Tricycla. The molecular analysis did not concur with this classification, but it clearly showed that B. spinosa does not have a close relationship with other species of Bougainvillea. It is also not the basal-most taxon but diverged earlier than the two major clades of Bougainvillea, the 'cultivated' Bougainvillea group (clade II) and the 'wild' Bougainvillea group (clade III).
Initially, it was assumed that B. praecox was synonymous with B. modesta due to similarities in appearance and lack of distinguishing characteristics, but plastid genome data showed that it has a closer relationship with the ornamental species, such as B. glabra and B. spectabilis. Sequence variation analysis further supported the close relationship of B. praecox to the cultivated Bougainvillea. High sequence similarity was observed between B. praecox and the reference B. glabra. In contrast, B. modesta had the greatest variation in sequences when compared to B. glabra, implying that B. modesta is not a close relative of B. glabra.
The sister-group relationship between the Bougainvillea glabra subclade and the B. spectabilis subclade was already established, since B. glabra and the cultivars are hardly differentiated from B. spectabilis [8]. Both the 'glabra' and 'spectabilis' subclades have thin, alternate leaves and large (2.5 to 4.5 cm), colorful, acute or acuminate bracts, and a constricted perianth tube ( Figure 5). Members of the 'glabra' subclade typically have glabrate to puberulent vegetative parts while the 'spectabilis' subclade can be characterized by having a fulvous to villous stem and a villous abaxial leaf surface [8,10]. Sequences deposited in Gen-Bank are mostly from cultivated plants and are identified as either B. glabra or B. spectabilis. In the B. glabra group, it was quite evident that the samples identified as B. arborea were closely associated to B. glabra. Bougainvillea arborea might be distinct from B. glabra by its tree-like habit (vs. scandent shrub), unarmed or sparsely armed with simple thorns (vs. armed with simple stout thorns), greenish-yellow perianth lobes (vs. yellowish-white or cream perianth lobes) (Figure 6), and obconical-obturbinoid or fusiform (vs. oblong) anthocarp and base of the perianth tube ( Figure 5). Further studies are needed to validate the exact relationship between B. arborea and B. glabra. On the other hand, Bougainvillea cultivar was within the 'spectabilis' group, since cultivars are usually crossed between the two species, B. glabra and B. spectabilis. Thereby, it is expected that most cultivars will be closer to either B. glabra or B. spectabilis.
The majority of the wild species of Bougainvillea grouped together in clade III. The species of Bougainvillea (B. berberidifolia, B. campanulata, B. infesta) with thin leaves arranged into fascicles or brachyblasts are members of this group ( Figure 7) [8,10]. Wild species of Bougainvillea with thin, alternate leaves such as B. stipitata and B. modesta also belong to clade III. Most of these wild species have smaller and unostentatious, normally white, greenish, or pale pink bracts, although the shade of color of the perianth lobes is more striking than in cultivated plants. Unlike the typical whitish or cream perianth lobes (Figure 6), wild species have brighter shades of green (B. stipitata, B. infesta), yellow (B. campanulata, B. modesta), or red (B. berberidifolia) [22,23].
Aside from the above-mentioned characteristics, there are no other unifying features that represent clade III. Perianth tubes are highly-variable and might be informative in differentiating wild species of Bougainvillea, but it is not a character that can be used to define the group (clade III). Thus, further morphological and anatomical studies may elucidate the relationships among the wild species of Bougainvillea. Nonetheless, analysis of SNPs and indels revealed high sequence similarities among the species. When aligned with B. glabra, large deletions were identified in the rps16 intron and a few intergenic spacers (trnR-AGC-trnN-GUU and rpl32-trnL-UAG) of all species in this clade. Small deletions were also noticeable in the matK and accD genes of these species. The deletions were not observed in sequences from the 'cultivated' Bougainvillea clade. thorns (vs. armed with simple stout thorns), greenish-yellow perianth lobes (vs. yellowish-white or cream perianth lobes) (Figure 6), and obconical-obturbinoid or fusiform (vs. oblong) anthocarp and base of the perianth tube ( Figure 5). Further studies are needed to validate the exact relationship between B. arborea and B. glabra. On the other hand, Bougainvillea cultivar was within the 'spectabilis' group, since cultivars are usually crossed between the two species, B. glabra and B. spectabilis. Thereby, it is expected that most cultivars will be closer to either B. glabra or B. spectabilis.   Aside from the above-mentioned characteristics, there are no other unifying features that represent clade III. Perianth tubes are highly-variable and might be informative in differentiating wild species of Bougainvillea, but it is not a character that can be used to define the group (clade III). Thus, further morphological and anatomical studies may elucidate the relationships among the wild species of Bougainvillea. Nonetheless, analysis of SNPs and indels revealed high sequence similarities among the species. When aligned with B. glabra, large deletions were identified in the rps16 intron and a few intergenic spacers (trnR-AGC-trnN-GUU and rpl32-trnL-UAG) of all species in this clade. Small deletions were also noticeable in the matK and accD genes of these species. The deletions were not observed in sequences from the 'cultivated' Bougainvillea clade.
Based on our analyses, several taxonomic relationships could be established. The classification proposed by Standley [10] was not supported in this study based on chloroplast genomes. Early divergence of Bougainvillea peruviana, B. pachyphylla, and B. spinosa was highly supported, thus making them the basal taxa in Bougainvillea. Specifically, high morphological and molecular similarities were observed between B. pachyphylla and B. peruviana (clade I). The remaining species of Bougainvillea diverged into two monophyletic clades, the predominantly 'cultivated' Bougainvillea group (clade II) and the 'wild' Bou- Based on our analyses, several taxonomic relationships could be established. The classification proposed by Standley [10] was not supported in this study based on chloroplast genomes. Early divergence of Bougainvillea peruviana, B. pachyphylla, and B. spinosa was highly supported, thus making them the basal taxa in Bougainvillea. Specifically, high morphological and molecular similarities were observed between B. pachyphylla and B. peruviana (clade I). The remaining species of Bougainvillea diverged into two monophyletic clades, the predominantly 'cultivated' Bougainvillea group (clade II) and the 'wild' Bougainvillea group (clade III). In addition, the present analyses did not support the previously proposed merging of B. praecox and B. modesta; B. modesta is clearly a species distinct from B. praecox as evidenced by the plastid genome data and perianth structure ( Figure 5). Bougainvillea praecox is sister to B. spectabilis and B. glabra, while B. modesta belongs to the 'wild' Bougainvillea clade. The analyses also confirmed that B. luteoalba is a synonym of B. modesta and B. stipitata var. grisebachiana is a synonym of B. stipitata. The B. arborea samples fell into the clade of B. glabra and resulted in a new synonymy under B. glabra var. obtusibracteata. The results of this study have taxonomic implications in the classification of Bougainvillea. Enumerated here, therefore, are the names of the species of Bougainvillea (and their synonyms) that we accept. Shrubs or small trees, often scandent, usually armed with simple or furcate thorns; leaves alternate or in brachyblasts, petiolate, entire; flowers perfect, either solitary and subtended by 3 bracts or typically in a 3-flowered, axillary inflorescence comprising 3 large, persistent, often brightly colored bracts with a flower borne on the inner surface of each bract, its pedicel confluent with the costa of the bract; perianth tubular, terete, usually constricted in the middle and ends in several induplicate-valvate or contorted lobes, the limb usually composed of glandular or non-glandular central lobes and adjacent commissural lobes; stamens 5-10, unequal to some extent, connate at the base into a cup-like structure; anthocarp woody, coriaceous, ribbed.

Taxonomic
Distribution: Native to Argentina, Bolivia, Brazil, Ecuador, Paraguay, and Peru. Ornamental species (Bougainvillea glabra and B. spectabilis) introduced to most tropical and subtropical regions for cultivation. The high-quality reads obtained were initially spliced in SPAdes 3.11.0-St. Petersburg genome assembler [32]. Using the default parameters (without the cutoff parameter), all the scaffolds that could be assembled from the clean data were spliced together. Then BlastN was performed with the published genome of Bougainvillea spectabilis. The comparison threshold was set to e-value 1 × 10 −10 and protein similarity threshold of 70%. The scaffolds that matched the genes were selected and the splicing coverage was sorted. The fragments with low coverage, which were obviously not included in the target genome, were removed. Subsequently, the collected target fragment sequences were extended and merged using PRICE software [33] to minimize the number of scaffolds. The number of iterations was set to 50. The results of iterative splicing were aligned to the original sequencing reads using Bowtie 2 [34]. The matched pairs of reads were then selected and re-spliced using SPAdes 3.11.0 [32].

SNPs and Indels Analysis
The variation among the plastid genomes of Bougainvillea was analyzed through SNPs (Single Nucleotide Polymorphisms) and indels (insertions and deletions) identification. SNPs and indels were identified in MUMmer 4 [19] and Geneious Prime 2020.2 [20] using B. glabra as the reference genome. The nonsynonymous (Ka) and synonymous (Ks) substitution rates of the protein-coding genes were also determined through the Selecton 2007 program [41].

Phylogenetic Analysis
To elucidate the phylogenetic relationships within Bougainvillea, 11 newly sequenced plastid genomes were included in the analysis, along with the eight sequences of Bougainvillea from previous studies, and six additional sequences of Nyctaginaceae from GenBank (Table S4). Four chloroplast genomes from the allied family Petiveriaceae were also used as outgroups. From these datasets, 79 protein-coding sequences were extracted and aligned using MAFFT v7.388 [42] software embedded in Geneious Prime 2020.2 [20]. When necessary, alignments were manually adjusted to remove ambiguous areas.
After the alignment, Maximum Likelihood (ML) analysis was carried out in RAxML 8.2.11 using the GTR+I+G nucleotide substitution model [43,44]. The appropriate model was determined through jmodeltest2 performed in CIPRES Gateway [45]. The consensus tree was inferred from 1000 replicates using Seguieria aculeata, Rivina humilis, Petiveria alliacea, and Monococcus echinophorus as outgroups. In addition, Bayesian Inference (BI) was also analyzed using MrBayes 3.2.6 with the general time-reversible model of DNA substitution and a gamma distribution rate variation across sites [46]. BI analyses were conducted in CIPRES Gateway [45] with the setting of four MCMCs running for one million generations with sampling every 1000 generations, and the first 25% discarded as burn-in. Branches with ML bootstrap support above 75 and Bayesian posterior probabilities (BPP) above 0.95 were regarded as significantly supported.

Morphological Analysis
Digital images of specimens of Bougainvillea from various herbaria (A, B, BR, CORD, E, F, GH, GOET, K, LPB, MA, MICH, MO, MPU, NY, P, S, US, USZ, W) were used in the morphological study. In addition, fresh specimens from the living collection of Bougainvillea in the Shenzhen Fairy Lake Botanical Garden were used for morphological observations and floral dissections. Photographs of additional species of Bougainvillea were also retrieved from the Flora of Argentina [22] and Flora of the World Online [23]. The terminologies used to describe the materials were mainly based on the Kew plant glossary [47]. The table of diagnostic characteristics (Table S5) was based primarily on direct observations, but published descriptions and protologues were also used to complete the table.
Supplementary Materials: The following supporting information can be downloaded at: https: //www.mdpi.com/article/10.3390/plants11131700/s1, Table S1: Genome features of Bougainvillea chloroplast genomes; Table S2: List of genes encoded by Bougainvillea chloroplast genomes; Table S3: Bougainvillea samples included in the study; Table S4: Data set included in the phylogenetic and comparative analyses of complete chloroplast DNA sequences (Bougainvillea, Nyctaginaceae); Table S5: Morphological comparison of Bougainvillea species; Figure S1: Insertion-Deletions (Indels) in the protein-coding genes of Bougainvillea chloroplast genomes. Funding: This research was supported by the Shenzhen Urban Management Bureau (Chen, 2001(Chen, , 2009; Shenzhen Science and Technology Innovation Commission (JCYJ20120615172425764), the Fourth National Survey of Chinese Traditional Medicine Resources (GZY-KJS-2018-004); the Shenzhen Key Laboratory of South Subtropical Plant Diversity, Fairy Lake Botanical Garden, Chinese Academy of Sciences (Chen, 2018(Chen, -2021; and the Key Laboratory of Plant Resource Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences (Deng, 2018(Deng, -2021.

Data Availability Statement:
The complete chloroplast genome sequences of Bougainvillea samples used in the study were deposited in the NCBI GenBank under accession numbers OM044392-OM044400, MW123899-MW123903.