Comparative chloroplast genomes: insights into the evolution of the chloroplast genome of Camellia sinensis and the phylogeny of Camellia

Abstract Background: Chloroplast genome resources can provide useful information for the evolution of plant species. Tea plant (Camellia sinensis) is among the most economically valuable member of Camellia. Here, we determined the chloroplast genome of the first natural triploid Chinary type tea (‘Wuyi narcissus’ cultivar of Camellia sinensis var. sinensis, CWN) and conducted the genome comparison with the diploid Chinary type tea (Camellia sinensis var. sinensis, CSS) and two types of diploid Assamica type teas (Camellia sinensis var. assamica: Chinese Assamica type tea, CSA and Indian Assamica type tea, CIA). Further, the evolutionary mechanism of the chloroplast genome of Camellia sinensis and the relationships of Camellia species based on chloroplast genome were discussed.Results: Comparative analysis showed the evolutionary dynamics of chloroplast genome of Camellia sinensis were the repeats and insertion-deletions (indels), and distribution of the repeats, indels and substitutions were significantly correlated. Chinese tea and Indian tea had significant differences in the structural characteristic and the codon usage of the chloroplast genome. Analysis of sequence characterized amplified region (SCAR) using sequences of the intergenic spacers (trnE/trnT) showed none of 292 different Camellia sinensis cultivars had similar sequence characteristic to triploid CWN, but the other four Camellia species did. Estimations of the divergence time showed that CIA diverged from the common ancestor of two Assamica type teas about 6.2 Mya (CI: 4.4-8.1 Mya). CSS and CSA diverged to each other about 0.8 Mya (CI: 0.4-1.5 Mya). Moreover, phylogenetic clustering was not exactly consistent with the current taxonomy of Camellia.Conclusions: The repeat-induced and indel-induced mutations were two important dynamics contributed to the diversification of the chloroplast genome in Camellia sinensis, which were not mutually exclusive. Chinese tea and Indian tea might have undergone different selection pressures. Chloroplast transfer occurred during the polyploid evolution in Camellia sinensis. In addition, our results supported the three different domestication origins of Chinary type tea, Chinese Assamica type tea and Indian Assamica type tea. And, the current classification of some Camellia species might need to be further discussed.

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Comparative chloroplast genomes: insights into the evolution of the chloroplast genome of Camellia sinensis and the phylogeny of Camellia

BMC Genomics ◽

10.1186/s12864-021-07427-2 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Li Li ◽

Yunfei Hu ◽

Min He ◽

Bo Zhang ◽

Wei Wu ◽

...

Keyword(s):

Chloroplast Genome ◽

Camellia Sinensis ◽

Evolutionary Dynamics ◽

Divergence Time ◽

Tea Plant ◽

Genome Comparison ◽

Induced Mutations ◽

Polyploid Evolution ◽

Chloroplast Genomes ◽

Indian Tea

Abstract Background Chloroplast genome resources can provide useful information for the evolution of plant species. Tea plant (Camellia sinensis) is among the most economically valuable member of Camellia. Here, we determined the chloroplast genome of the first natural triploid Chinary type tea (‘Wuyi narcissus’ cultivar of Camellia sinensis var. sinensis, CWN) and conducted the genome comparison with the diploid Chinary type tea (Camellia sinensis var. sinensis, CSS) and two types of diploid Assamica type teas (Camellia sinensis var. assamica: Chinese Assamica type tea, CSA and Indian Assamica type tea, CIA). Further, the evolutionary mechanism of the chloroplast genome of Camellia sinensis and the relationships of Camellia species based on chloroplast genome were discussed. Results Comparative analysis showed the evolutionary dynamics of chloroplast genome of Camellia sinensis were the repeats and insertion-deletions (indels), and distribution of the repeats, indels and substitutions were significantly correlated. Chinese tea and Indian tea had significant differences in the structural characteristic and the codon usage of the chloroplast genome. Analysis of sequence characterized amplified region (SCAR) using sequences of the intergenic spacers (trnE/trnT) showed none of 292 different Camellia sinensis cultivars had similar sequence characteristic to triploid CWN, but the other four Camellia species did. Estimations of the divergence time showed that CIA diverged from the common ancestor of two Assamica type teas about 6.2 Mya (CI: 4.4–8.1 Mya). CSS and CSA diverged to each other about 0.8 Mya (CI: 0.4–1.5 Mya). Moreover, phylogenetic clustering was not exactly consistent with the current taxonomy of Camellia. Conclusions The repeat-induced and indel-induced mutations were two important dynamics contributed to the diversification of the chloroplast genome in Camellia sinensis, which were not mutually exclusive. Chinese tea and Indian tea might have undergone different selection pressures. Chloroplast transfer occurred during the polyploid evolution in Camellia sinensis. In addition, our results supported the three different domestication origins of Chinary type tea, Chinese Assamica type tea and Indian Assamica type tea. And, the current classification of some Camellia species might need to be further discussed.

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Comparative chloroplast genome s: insights into the evolution of the chloroplast genome of Camellia sinensis and the phylogeny of Camellia

10.21203/rs.3.rs-36917/v3 ◽

2021 ◽

Author(s):

LI li ◽

Yunfei Hu ◽

Min He ◽

Bo Zhang ◽

Wei Wu ◽

...

Keyword(s):

Chloroplast Genome ◽

Camellia Sinensis ◽

Evolutionary Dynamics ◽

Divergence Time ◽

Tea Plant ◽

Genome Comparison ◽

Induced Mutations ◽

Polyploid Evolution ◽

Sequence Characterized Amplified Region ◽

Indian Tea

Abstract Background: Chloroplast genome resources can provide useful information for the evolution of plant species. Tea plant (Camellia sinensis) is among the most economically valuable member of Camellia. Here, we determined the chloroplast genome of the first natural triploid Chinary type tea (‘Wuyi narcissus’ cultivar of Camellia sinensis var. sinensis, CWN) and conducted the genome comparison with the diploid Chinary type tea (Camellia sinensis var. sinensis, CSS) and two types of diploid Assamica type teas (Camellia sinensis var. assamica: Chinese Assamica type tea, CSA and Indian Assamica type tea, CIA). Further, the evolutionary mechanism of the chloroplast genome of Camellia sinensis and the relationships of Camellia species based on chloroplast genome were discussed.Results: Comparative analysis showed the evolutionary dynamics of chloroplast genome of Camellia sinensis were the repeats and insertion-deletions (indels), and distribution of the repeats, indels and substitutions were significantly correlated. Chinese tea and Indian tea had significant differences in the structural characteristic and the codon usage of the chloroplast genome. Analysis of sequence characterized amplified region (SCAR) using sequences of the intergenic spacers (trnE/trnT) showed none of 292 different Camellia sinensis cultivars had similar sequence characteristic to triploid CWN, but the other four Camellia species did. Estimations of the divergence time showed that CIA diverged from the common ancestor of two Assamica type teas about 6.2 Mya (CI: 4.4-8.1 Mya). CSS and CSA diverged to each other about 0.8 Mya (CI: 0.4-1.5 Mya). Moreover, phylogenetic clustering was not exactly consistent with the current taxonomy of Camellia. Conclusions: The repeat-induced and indel-induced mutations were two important dynamics contributed to the diversification of the chloroplast genome in Camellia sinensis, which were not mutually exclusive. Chinese tea and Indian tea might have undergone different selection pressures. Chloroplast transfer occurred during the polyploid evolution in Camellia sinensis. In addition, our results supported the three different domestication origins of Chinary type tea, Chinese Assamica type tea and Indian Assamica type tea. And, the current classification of some Camellia species might need to be further discussed.

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Comparative chloroplast genomes: insights into the evolution of the chloroplast genome of Camellia sinensis and the phylogeny of Camellia

10.21203/rs.3.rs-36917/v2 ◽

2020 ◽

Author(s):

Li li ◽

Yunfei Hu ◽

Min He ◽

Bo Zhang ◽

Wei Wu ◽

...

Keyword(s):

Chloroplast Genome ◽

Camellia Sinensis ◽

Evolutionary Dynamics ◽

Divergence Time ◽

Tea Plant ◽

Genome Comparison ◽

Induced Mutations ◽

Sequence Characterized Amplified Region ◽

Chloroplast Genomes ◽

Indian Tea

Abstract Background: Chloroplast genome resources can provide useful information for the evolution of plant species. Tea plant (Camellia sinensis) is among the most economically valuable member of Camellia. Here, we determined the chloroplast genome of the first natural triploid Chinary type tea ( ‘Wuyi narcissus’ cultivar of Camellia sinensis var. sinensis, CWN) and conducted the genome comparison with the diploid Chinary type tea (Camellia sinensis var. sinensis, CSS) and two types of diploid Assamica type teas (Camellia sinensis var. assamica: Chinese Assamica type tea, CSA and Indian Assamica type tea, CIA). Further, the evolutionary mechanism of the chloroplast genome of Camellia sinensis and the relationships of Camellia species based on chloroplast genome were discussed.Results: Comparative analysis showed the evolutionary dynamics of chloroplast genome of Camellia sinensis were the repeats and insertion-deletions (indels), and distribution of the repeats, indels and substitutions were significantly correlated. Chinese tea and Indian tea had significant differences in the structural characteristic and the codon usage of the chloroplast genome. Analysis of sequence characterized amplified region (SCAR) using sequences of the intergenic spacers (trnE/trnT) showed none of 292 different Camellia sinensis cultivars had similar sequence characteristic to triploid CWN, but the other four Camellia species did. Estimations of the divergence time showed that CIA diverged from the common ancestor of two Assamica type teas about 6.2 Mya (CI: 4.4-8.1 Mya). CSS and CSA diverged to each other about 0.8 Mya (CI: 0.4-1.5 Mya). Moreover, phylogenetic clustering was not exactly consistent with the current taxonomy of Camellia.Conclusions: The repeat-induced and indel-induced mutations were two important dynamics contributed to the diversification of the chloroplast genome in Camellia sinensis, which were alternative but not mutually exclusive. Chinese tea and Indian tea might have undergone different selection pressures. Chloroplast transfer occurred during the polyploidy in Camellia sinensis. In addition, our results supported the three different domestication origins of Chinary type tea, Chinese Assamica type tea and Indian Assamica type tea. And, the current classification of some Camellia species might need to be further discussed.

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Comparative chloroplast genomes of the tea plants and the implications for the different origins of the two Assam teas

10.21203/rs.3.rs-36917/v1 ◽

2020 ◽

Author(s):

LI li ◽

Yunfei Hu ◽

Min He ◽

Bo Zhang ◽

Yongcong Hong ◽

...

Keyword(s):

Codon Usage ◽

Chloroplast Genome ◽

Camellia Sinensis ◽

Evolutionary Relationship ◽

Tea Plant ◽

Sequence Difference ◽

Indel Mutation ◽

Chloroplast Genomes ◽

Tea Plants ◽

Indian Tea

Abstract Background Tea plants belong to the genus Camellia, whose species are taxonomically complex due to frequent hybridization and polyploidy nature. The genetic genealogy of Camellia has always been a focus of botanical and ecological research, including a debate about whether Assam tea has two different domestication origins (Chinese Assam type and Indian Assam type). The chloroplast genome resources were able to provide useful data for the analysis of the plastome evolutionary relationship and species classification. Here, we determined the first chloroplast genome of the natural triploid tea plant (Camellia sinensis cv. Wuyi Narcissus) and conducted the genome comparison with Chinese type tea (Camellia sinensis var. sinensis), Chinese Assam type tea (Camellia sinensis var. assamica) and Indian Assam type tea (Camellia assamica) to improve our understanding of the evolutionary mechanism and the taxonomic classification of Camellia. Results This study presented detailed sequences and structural variations of chloroplast genomes of four tea plants. The chloroplast genome of the natural triploid tea showed no obvious sequence difference from that of other two types of Chinese teas, while that of Chinese tea and Indian tea was significant sequence difference. The natural selection probably dominated in shaping the codon bias of the chloroplast genome in tea plant, and the codon usage distribution of genome in Indian tea was obviously different from that in Chinese tea. The phylogenetic status of Chinese and Indian Assam teas was in the different branches of the tea plant. Phylogenetic tree clustering was not consistent with the current some taxonomy of Camellia. Conclusions The sequence variation of the chloroplast genome of tea plant was mainly ascribed to the expansion and contraction of the border regions (IR/ SC), which were mainly due to the sequence repeat and indel mutation events of the genome. The codon usage pattern and phylogenetic analysis supported Chinese Assam type and Indian Assam type tea might have different domestication origins and suggested the current some taxonomy of Camellia might need revision.

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Chloroplast phylogenomics and the dynamic evolution of Santalum (Santalaceae)

10.21203/rs.3.rs-154608/v1 ◽

2021 ◽

Author(s):

Xiaojin Liu ◽

Daping Xu ◽

Zhou Hong ◽

Ningnan Zhang ◽

Zhiyi Cui

Keyword(s):

Chloroplast Genome ◽

Evolutionary Dynamics ◽

Divergence Time ◽

Major Type ◽

Time Analysis ◽

Chloroplast Genomes ◽

Extant Species ◽

History Of ◽

Insight Into ◽

Simple Sequence

Abstract Background Santalum (Santalaceae, sandalwood) is a hemiparasitic genus including approximately 15 extant species. It is known for its aromatic heartwood oil, which is used in incense and perfume. Demand for sandalwood-based products has led to drastic over-harvesting, and wild Santalum populations are now threatened. Knowledge of the phylogenetic relationships and genetic diversity will be critical for the conservation and proper management of this genus. Here, we sequenced the chloroplast genome of 11 Santalum species. The data were then used to investigate the chloroplast genome evolutionary dynamics and relationships and divergence time within Santalum and related species. Results The Santalum chloroplast genome contains the typical quadripartite structures, ranging from 143,291 to 144,263 bp. The chloroplast genome contains 124 genes. The whole set of ndh genes and the infA gene were found to lose their function. Between 17 and 31 SSRs were found in the Santalum chloroplast genome, and mononucleotide simple sequence repeats (SSRs) were the major type. The P-distance among the Santalum species was 0.0003 to 0.00828. Three mutation hotspot regions, 14 small inversions, and 460 indels events were discovered in the Santalum chloroplast genome. Our phylogenomic assessment provides improved resolution compared to past analyses. Our divergence time analysis shows that the crown age of Santalum was 8.46 Mya, the first divergence occurred around 6.97 Mya, and diversification was complete within approximately 1 Mya. Conclusions By sequencing the 12 chloroplast genomes of Santalum, we gain insight into the evolution of its chloroplast genomes. The chloroplast genome sequences had sufficient polymorphic information to elucidate the evolutionary history of Santalum.

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Comparative and Phylogenetic Analysis of the Complete Chloroplast Genome of Santalum (Santalaceae)

Forests ◽

10.3390/f12101303 ◽

2021 ◽

Vol 12 (10) ◽

pp. 1303

Author(s):

Xiaojin Liu ◽

Daping Xu ◽

Zhou Hong ◽

Ningnan Zhang ◽

Zhiyi Cui

Keyword(s):

Chloroplast Genome ◽

Phylogenetic Relationships ◽

Evolutionary Dynamics ◽

Divergence Time ◽

Purifying Selection ◽

Complete Chloroplast Genome ◽

Chloroplast Genomes ◽

Branch Model ◽

Extant Species ◽

Ndh Genes

Santalum (Santalaceae, sandalwood) is a hemiparasitic genus that includes approximately 15 extant species. It is known for its aromatic heartwood oil, which is used in incense and perfume. Demand for sandalwood-based products has led to drastic over-harvesting, and wild Santalum populations are now threatened. Knowledge of phylogenetic relationships will be critical for the conservation and proper management of this genus. Here, we sequenced the chloroplast genome of 11 Santalum species. The data were then used to investigate chloroplast genome evolutionary dynamics and relationships and divergence time within Santalum and related species. The Santalum chloroplast genome contains typical quadripartite structures, ranging from 143,291 to 144,263 bp. The chloroplast genome contains 110 unique genes. The whole set of ndh genes and the infA gene were found to lose their functions. The P-distance among the Santalum species was 0.0003 to 0.00828. Three mutation hotspot regions, 14 small inversions, and 460 indels events were discovered in the Santalum chloroplast genome. Branch-model-based selection analyses showed that the Santalum species were under widespread purifying selection. Our phylogenomic assessment provides an improved resolution to the phylogenetic relationships of Santalum compared to the past analyses. Our divergence time analysis showed that the crown age of Santalum was 8.46 Mya (million years ago), the first divergence occurred around 6.97 Mya, and diversification was completed approximately 1 Mya. By sequencing the 11 Santalum species chloroplast genomes, we identified the variations in the Santalum chloroplast genomes. Using the chloroplast genome sequences, phylogeny and divergence time analyses discovered that the Santalum species were likely to originate due to radiation evolution, and most speciation events occurred less than 1 Mya.

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The complete chloroplast genome sequence of economical standard tea plant, Camellia sinensis L. cultivar Sangmok, in Korea

Mitochondrial DNA Part B ◽

10.1080/23802359.2020.1790311 ◽

2020 ◽

Vol 5 (3) ◽

pp. 2835-2836

Author(s):

Dong-Jun Lee ◽

Chang-Kug Kim ◽

Tae-Ho Lee ◽

So-Jin Lee ◽

Doo-Gyung Moon ◽

...

Keyword(s):

Chloroplast Genome ◽

Genome Sequence ◽

Camellia Sinensis ◽

Tea Plant ◽

Complete Chloroplast Genome ◽

Chloroplast Genome Sequence

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Phylogenic study of Lemnoideae (duckweeds) through complete chloroplast genomes for eight accessions

PeerJ ◽

10.7717/peerj.4186 ◽

2017 ◽

Vol 5 ◽

pp. e4186 ◽

Cited By ~ 5

Author(s):

Yanqiang Ding ◽

Yang Fang ◽

Ling Guo ◽

Zhidan Li ◽

Kaize He ◽

...

Keyword(s):

Chloroplast Dna ◽

Chloroplast Genome ◽

Morphological Characters ◽

Repeat Sequence ◽

Genome Comparison ◽

Protein Coding ◽

Phylogenetic Studies ◽

Chloroplast Genomes ◽

Effective Option ◽

Total Dna

Background Phylogenetic relationship within different genera of Lemnoideae, a kind of small aquatic monocotyledonous plants, was not well resolved, using either morphological characters or traditional markers. Given that rich genetic information in chloroplast genome makes them particularly useful for phylogenetic studies, we used chloroplast genomes to clarify the phylogeny within Lemnoideae. Methods DNAs were sequenced with next-generation sequencing. The duckweeds chloroplast genomes were indirectly filtered from the total DNA data, or directly obtained from chloroplast DNA data. To test the reliability of assembling the chloroplast genome based on the filtration of the total DNA, two methods were used to assemble the chloroplast genome of Landoltia punctata strain ZH0202. A phylogenetic tree was built on the basis of the whole chloroplast genome sequences using MrBayes v.3.2.6 and PhyML 3.0. Results Eight complete duckweeds chloroplast genomes were assembled, with lengths ranging from 165,775 bp to 171,152 bp, and each contains 80 protein-coding sequences, four rRNAs, 30 tRNAs and two pseudogenes. The identity of L. punctata strain ZH0202 chloroplast genomes assembled through two methods was 100%, and their sequences and lengths were completely identical. The chloroplast genome comparison demonstrated that the differences in chloroplast genome sizes among the Lemnoideae primarily resulted from variation in non-coding regions, especially from repeat sequence variation. The phylogenetic analysis demonstrated that the different genera of Lemnoideae are derived from each other in the following order: Spirodela, Landoltia, Lemna, Wolffiella, and Wolffia. Discussion This study demonstrates potential of whole chloroplast genome DNA as an effective option for phylogenetic studies of Lemnoideae. It also showed the possibility of using chloroplast DNA data to elucidate those phylogenies which were not yet solved well by traditional methods even in plants other than duckweeds.

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Comparative Chloroplast Genome Analysis of Medicinally Important Veratrum (Melanthiaceae) in China: Insights into Genomic Characterization and Phylogenetic Relationships

10.21203/rs.3.rs-117897/v1 ◽

2020 ◽

Author(s):

Ying-min Zhang ◽

Li-jun Han ◽

Ying-Ying Liu ◽

Cong-wei Yang ◽

Xing Tian ◽

...

Keyword(s):

Chloroplast Genome ◽

Phylogenetic Analyses ◽

Genome Structure ◽

Blood Stasis ◽

Genome Comparison ◽

Phylogenetic Study ◽

Species Classification ◽

Chloroplast Genomes ◽

Genomic Characterization ◽

Cp Genome

Abstract Background: Veratrum is a genus of perennial herbs that are widely used as traditional Chinese medicine for emetic, resolving blood stasis and relieve pain. However, the species classification and the phylogenetic relationship of the genus Veratrum have long been controversial due to the complexity of morphological variations. Knowledge on the infrageneric relationships of the genus Veratrum can be obtained from their chloroplast genome sequences and increase the taxonomic and phylogenetic resolution.Methods: Total DNA was extracted from ten species of Veratrum and subjected to next-generation sequencing. The cp genome was assembled by NOVOPlasty. Genome annotation was conducted using the online tool DOGMA and subsequently corrected by Geneious Prime. Then, genomic characterization of the Veratrum plastome and genome comparison with closely related species was analyzed by corresponding software. Moreover, phylogenetical trees were reconstructed, based on the 29 plastomes by maximum likelihood (ML) and Bayesian inference (BI) methods.Results: The whole plastomes of Veratrum species possess a typical quadripartite structure, ranging from 151,597 bp to 153,711 bp in size and comprising 135 genes. The gene order, content, and genome structure were nearly identical with a few exceptions across the Veratrum chloroplast genomes. The total number of simple sequence repeats (SSRs) ranged from 31 to 35, and of large sequence repeats (LSRs) ranged from 65 to 71. Seven highly divergent regions (rpoB-trnC, trnT-trnL, trnS-trnG, psbC-psbZ, psbI, ycf1, and ndhF) were identified that can be used for DNA barcoding in the genus of Veratrum. Phylogenetic analyses based on 29 plastomes strongly supported the monophyly of Veratrum. The circumscription and relationships of infrageneric taxa of Veratrum were well evaluated with high resolutions. Conclusions: Our study identified and analyzed the cp genome features of ten Veratrum species, and suggested high effectivity of chloroplast complete genome in resolving generic circumscription in Veratrum. These results will facilitate the identification, taxonomy, and utilization of Veratrum plants as well as the phylogenetic study of Melanthiaceae simultaneously.

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Multifunctional Green Synthetic Hematite (α-Fe2O3) Nanoparticles Mediated by Camellia Sinensis (Indian Tea Plant) Extracts towards Antioxidant and Antiproliferative Activities against MCF-7 Cell Lines

Journal of Pharmaceutics and Therapeutics ◽

10.18314/jpt.v6i1.2028 ◽

2020 ◽

Vol 6 (1) ◽

pp. 355-367

Author(s):

Pradhan D ◽

Behera B ◽

Samantaray A ◽

Tripathy G ◽

Pradhan S

Keyword(s):

Electron Microscopy ◽

Camellia Sinensis ◽

Plant Extracts ◽

Magnetic Measurements ◽

Tea Plant ◽

Fe2o3 Nanoparticles ◽

M Cell ◽

Medicinal Uses ◽

Indian Tea ◽

Mcf 7

Among nanoparticles used for medical applications, Camellia Sinensis Nanoparticles (CSNPs) are among the least investigated. This study was undertaken to develop CSNPs by green synthesis using Camellia sinensis tea (Theaceae) plant extract to produce the NPs. The Camellia sinensis, Indian tea plant used from ancient time to increase appetite. Other medicinal uses have also been employed for the synthesis of super paramagnetic α Fe2O3 nanoparticles (NPs). The plant extracts revealed the phenolic groups bifunctional nature and capping nature through the –OH bonding over the nanoparticles (NPs) surface. The prepared nanoparticles (NPs) shows α-Fe2O3 phase among iron oxides and spherical morphology with an average size around 5 nm. The magnetic measurements proved the superparamagnetic behaviour of NPs with non-saturating MS value of 8.5 emu/g at room temperature (300 K). The CSNPs were characterized by UV-V is spectroscopy and X-ray Diffractometry, and evaluated with Transmission Electron Microscopy (TEM), Scanning Electron Microscopy (SEM) and Fourier Transform Infrared (FTIR). The CSNPs were spherical (size 7-20 nm) and contained phenols and flavonoids acquired from the Camellia sinensis extract. CSNPs has good 1-Diphenyl-2-Picrylhydrazyl (DPPH), OH, and NO scavenging properties. MTT assay showed that CSNPs (IC50 = 0.006 μM) were more antiproliferative toward the human MCF-7 cells than the Camellia sinensis tea extract (IC50 = 0.894 μM), Gemcitabin (IC50 = 2.133 μM). The anticancer cell effects of CSNPs on MCF 7 are mediated through the induction of apoptosis and G2/M cell-cycle arrest.

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