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Deciphering Species Relationships and Evolution in Chenopodium Through Research Article Deciphering species relationships and evolution in Chenopodium through sequence variations in nuclear internal transcribed spacer region and amplified fragment length polymorphism in nuclear DNA Nikhil K. Chrungooa,*, Rajkumari Jashmi Devia†, Shailendra Goelb, Kamal Dasb a Department of Botany, Centre for Advanced Studies, North-Eastern Hill University, Shillong -793022 (India) b Department of Botany, University of Delhi, Delhi – 110 007 (India) *Corresponding author: Department of Botany, Centre for Advanced Studies, North-Eastern Hill University, Shillong – 793 022 (India), Tel: ++91 364 2722 211, email: [email protected]; [email protected] †Present address: Institute of Bioresources and Sustainable Development, Takyelpat, Imphal, Manipur- 795 001 (India) 1 Abstract Evaluation of sequence variations in the ITS region of nineteen accessions, comprising of 11 accessions of C. quinoa, 8 accessions of C. album and 165 retrieved sequences of different species of Chenopodium belonging to sub-family Chenopodioideae revealed a higher intraspecific genetic diversity in Himalayan C. album than that in C. quinoa. ITS and AFLP profiles of the accessions suggest the existence of accessions of Himalayan C. album as heteromorphs of the same species rather than a heterogenous assemblage of taxa. While the evolutionary relationship reconstructed from variations in 184 sequences of ITS region from species belonging to Chenopodiaceae, Amaranthaceae, Polygonaceae and Nelumbonaceae established a paraphyletic evolution of family Chenopodiaceae, it also revealed a monophyletic evolution of Chenopodieae I. The reconstruction also established five independent lineages of the sub-family Chenopodioideae with C. album as a sister clade of C. quinoa within the tribe Chenopodieae I. The results also indicate a much younger age of Himalayan Chenopods (C. album) than the reported crown age of Chenopodieae I. Key words Chenopodium, Chenopodioideae, ITS, AFLP, time-measured phylogenetic tree, evolutionary divergence, Running title: Species relationships and evolution in Chenopodium Abbreviations 2 ITS, Internal transcribed spacer; AFLP, Amplified fragment length polymorphism; DAMD, Direct Amplification of Minisatellite DNA; ISSR, Inter Simple Sequence Repeats; PIC, Polymorphic information content; myr, million years; mya, million years ago. Introduction Chenopodium is one of the taxonomically most complex genus. It belongs to the subfamily Chenopodioideae within the family Chenopodeace. The highly polymorphic habit of species within this genus has caused many difficulties in their proper taxonomic identification. Taxonomic identification of Chenopodium has been controversial because of the highly polymorphic leaf shape, floral structure, and seed morphology (La Duke and Crawford, 1979; Kurashige and Agrawal, 2005). While Wilson and Manhart (1993) have described the genus Chenopodium as a “taxonomic receptacle”, Rahiminejad and Gornall (2004) have described it as a complex group which lacked good morphological characteristics to distinguish between species. Most of the work on genetic diversity and phylogeny in Chenopodium has focused on C. quinoa and C. berlandieri subsp. nuttalliae (Ruas et al. 1999; Gangopadhyay and Mukherjee 2002) and only a few studies have been carried out on its other important species including C. album. Previous studies aimed at elucidating this taxonomic complex on the basis of cytology (Mehra and Malik 1963; Mukherjee 1986), karyotypic analysis (Bhargava et al. 2006; Kolano et al. 2008), flavonoids (Rahiminejad and Gornall 2004), RAPD profiles (Ruas et al. 1999; Gangopadhyay et al. 2002; Rana et al. 2010), DAMD (Rana et al. 2010) and ISSR markers (Rana et al. 2011) clearly indicate the existence of C. album as the most polymorphic species of the genus Chenopodium. Bhargava et al. (2006) and Rana et al. (2010) have suggested it to be aggregate taxon, thereby confusing its identity vis- a- vis Linnaean C. album. C. quinoa is an allotetraploid (2n = 4× = 36) with an estimated genome size of approximately 1.5 Gbp (Palomino et al., 2008; Kolano et al., 2016). On the other hand C. album is known as a complex of diploid (2n=18), tetraploid (2n=36) or hexaploid (2n=54) cytotypes with endopolyploidy and autopolyploidy as the origin of polyploidy (Kolano et al. 2008). Limited genetic resources in quinoa have long been considered as a major factor hindering molecular marker-assisted breeding (Jarvis et al., 2008). While the subfamily Chenopodiaceae has been considered to be monophyletic on the basis of sequence data of chloroplast rbcL (Kadereit et al., 2003) and matK/trnK (Müller and Borsch, 2005) genes, Fuentes-Bazan et al. (2012b) have argued that Chenopodium, as tradtionally recognized, consists of six independent lineages. The arguement was based on sequence diversity in plastid trnL-F and nuclear ITS regions of different species of this genus. Walsh et al. (2015) have, however, identified two distinct polyploid lineages out of which one lineage comprised of American tetraploid species and the other of Eastern Hemisphere hexaploid species. Thus, phylogenetic relationships amongst major lineages within Chenopodiaceae still remains poorly understood. Materials and Methods Plant materials Seeds of nineteen accessions of Chenopodium (Table 1) were procured from National Bureau of Plant Genetic resources, NBPGR, Shimla (India). The accessions were chosen on the basis of variations in colour, shape and arrangement of their leaves; colour, shape and surface morphology of their seeds; texture and type of 3 pollen grains. The selection of accessions was based on Devi and Chrungoo (2015). Plants of each accession were raised to full maturity in the experimental garden of the North Eastern Hill University, Shillong. PCR amplification of ITS region Genomic DNA, to be used as a template for PCR, was isolated from 10 day old etiolated seedlings of all the accessions following the method of Murray and Thomson (1980). PCR amplification of ITS region from genomic DNA of each accession was carried out with the forward (ITS5: 5´GGAAGTAAAAGTCGTAACAAGG3´) and reverse (ITS4: 5´TCCTCCGCTTATTGATATGC3´) primers designed by White et al. (1990). The reaction mixtures for amplification were optimized with 1mM MgCl2, 0.4mM dNTPs, 0.03U Taq Polymerase, 0.2pmols primers and 50ng of the template DNA. Amplification was performed in a thermal cycler programmed to one cycle of “hot start” (94°C); 35 cycles of denaturation (94°C, 1.0 min); annealing (50°C, 1 min) and extension (72°C, 1 min) and one final step of chain elongation at 72°C, 10 min. Each reaction mixture was electrophoresed on 1.2% agarose gel. The amplicons were visualized under UV light in ChemiDoc XRS+ system (Bio-Rad) after staining the gels with 0.5µg ml-1 ethidium bromide. The amplified DNA fragments were eluted from the gel and purified with QIA quick Gel Extraction Kit (QIAGEN India Pvt. Ltd.) following the manufacturer’s protocol. The precipitated DNA was pelletted by centrifuging at 13,000 rpm for 20 minutes at 4°C, washed twice with 70% alcohol and vacuum dried. The dried samples were dissolved in sterile distilled water. Nucleotide sequencing Nucleotide sequencing of each amplified DNA was carried out by capillary gel electrophoresis in ABI 3130 automated sequencer (Applied Biosystems) using POP-7 (Performance Optimzed Polymer) as the resolving matrix. Prior to sequencing, each amplicon was subjected to cycle sequencing with individual primers using the BigDye terminator v3.1 cycle sequencing kit (Thermo Fischer Scientific) as per the manufacturer’s protocol. The cycle sequencing protocol comprised of one cycle of hot start (96°C, 1 min), 35 cycles of denaturation (96°C, 10sec), annealing (Ta, 2 min) and chain extension (60°C, 3min). DNA was precipitated from the amplified reaction mixture by adding 25µl of absolute alcohol and 1.0µl of 125mM EDTA. The precipitated DNA was pelletted by centrifugation at 13,000rpm for 20 minutes at 4°C, washed twice with cold 70% alcohol and vacuum dried. The samples were denatured by addition of 10µl of formamide and heating at 96°C for 2 minutes prior to nucleotide sequencing. Sequence analysis The nucleotide sequences were analyzed by BLAST (http://www.ncbi.nlm.nih.gov/Blast) to determine their homology with other known sequences in the Genbank databases. Statistical analyses for determining inter/intra- specific sequence diversity was carried out using SeqState v.1.21(Muller 2005). Multiple sequence alignments to determine conserved sites (CS), variable sites (VS), parsimony informative sites (PIS), singleton sites (SS), and transition/transversion ratio and nucleotide pair frequencies viz. identical pair (ip), transitional pair (Ts) and transversional pair (Tv) were generated with MEGA 6.06 (Tamura et al.2011). 4 Compensatory bases changes in predicted secondary structure of ITS2 The secondary structure of ITS2 was predicted using Vienna RNA web servers (Vienna RNA package, version 2.1.9) at default energy and temperature (37ºC) with no manual modification and optimization in sequences. Compensatory base changes (CBCs), which are defined as base changes in a paired region of a primary RNA transcript when both nucleotides of a paired site mutate while the pairing itself is maintained (Gutell et al., 1994), were analyzed in the predicted secondary structure of ITS2 using CBC analyzer 1.1(Wolf et al. 2005). AFLP analysis AFLP analysis of DNA from the accessions of Chenopodium was carried out with LI-COR4300 DNA analyzer following the
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