Complete mitogenome structure and phylogenetic implications of the first Indian yak breed- Arunachali (Poephagus grunniens L.)

doi:10.21203/rs.3.rs-4358283/v1

Arunachali is the first registered breed of yak in India inhabiting Tawang and West Kameng districts of Arunachal Pradesh. Arunachali yak breed accounts for half the yak population in India, however, the number has been declining. In order to conserve and propagate this majestic and unique animal, this study reports the first ever whole mitogenome of an Indian yak breed. The mitogenome of Arunachali yak was found to be circular and double stranded with a length of 16,324 bp comprising 13 protein coding genes (PCGs), 22 tRNAs, 2 rRNAs and an 894bp non-coding control region (D-loop). Out of the 37 genes, 29 genes were encoded on H-strand and 8 on the L-strand. The overall nucleotide composition was A = 33.70%, T = 27.28%, G = 13.21% and C = 25.80% with an AT biasness. Phylogenetic analysis was done with three datasets involving 27 whole mitogenome of Chinese yak breeds and a Bos indicus outgroup sequence. The Arunachali yak shows same ancestry with the other yak breeds and more closeness to Jinchuan yak based on D-loop sequence. The findings of this study elucidate the mitochondrial genomic architecture of Arunachali yak and its evolutionary status along with providing basis for characterisation and formulation of specific breeding policies for Indian yaks.

Biological sciences/Biotechnology

Biological sciences/Evolution

Biological sciences/Genetics

Biological sciences/Molecular biology

Arunachali yak

Indian yak

mitogenome

breed conservation

phylogeny

Yak (Bos grunniens) is an evolutionarily unique species found across the Himalayan region and adapted to one of the most extreme climatic conditions on the planetat an altitude of 3000 to 6000 m above msl [1-3]. In India, yaks are found in the states of Sikkim, Himachal Pradesh, Ladakh and Arunachal Pradesh. The population of yak in India is around 58,000, of which half of the populace is concentrated in Arunachal Pradesh [4]. In the regions where yak is found, they become inextricably intertwined to the social, cultural and economic life of the transhumant pastoralist communities [3,5]. One such community of India, is the Brokpa of the north-eastern state of Arunachal Pradesh who depends almost entirely on yak and its by-products for their livelihood [6].

Arunachali (Poephagus grunniens L.) is the first and lone registered yak breed of the country [7] and endemic to Tawang and West Kameng districts of Arunachal Pradesh [3,8]. They are reared for milk, meat, fibre, manure and as a source of transportation in the unforgiving terrains of the trans-Himalayan region [9-11]. These animals are medium sized with compact angular bodies, strong short legs and can be massive with adult body weight of upto 410 kg in males and 270 kg in females [8]. Arunachali yaks are excellent pack animals in the extremely harsh climatic and environmental condition of the high altitudes. They can comfortably cover a distance of 7 km with a load between 25-35% of their live bodyweight without incurring any adverse physiological effects [12]. However, the population of yak has been dwindling due to various reasons associated with pastoralist lifestyle with little to no economic dividends in this modern era [3]. Therefore, it becomes pertinent to explore the unrevealed genome of this distinct germplasm to gain insights for improvement and propagation of the breed.

Mitochondrial genome (mitogenome) has been considered an ideal molecular marker for genetic diversity studies, phylogenetic inference and inferring evolutionary history of animals at least from the matrilineal side [13,14]. With the advancements in high-throughput sequencing techniques, complete mitogenomes have been characterised and efficiently used to study the domestication and phylogenetic relationship of various yak breeds [15-20] and other vertebrates [21-25]. However, all these studies lack representation of Indian yak and till date there is no documentation of the complete mitochondrial genome of Arunachali yak. We report a comprehensive mitogenome architecture of Arunachali yak and establish its genetic diversity and evolutionary status thereby providing basis for formulating breed specific conservation and breeding strategies.

Sample collection: The sample for this study was collected from yak farm of ICAR-National Research on Yak located at Nyukmadung, West Kameng District, Arunachal Pradesh situated at an altitude of 2750 m above msl (27°25'13.5"N 92°08'33.4"E). Approximately 20 ml of whole blood was collected from the jugular vein of a 6 years old female yak in K3 EDTA vials and stored at -80°C until DNA isolation.

DNA isolation, sequencing and assembly: High molecular weight genomic DNA (gDNA) was isolated using Blood & Cell Culture DNA Midi Kit (QIAGEN, Germany; Cat no.-13343) and quantified Qubit 4.0 fluorometer (Thermofisher #Q33238, Thermofisher Scientific, Massachusetts, USA) using DNA HS assay kit (Thermofisher #Q32851, Thermofisher Scientific, Massachusetts, USA). Purity of isolated gDNA was checked using NanoDrop 2000 (Thermofisher Scientific, Massachusetts, USA) and integrity was assessed on 1% agarose gel (Lonza, Basel, Cat No:50004). Additionally, size distribution was checked on Agilent FEMTO pulse analyser (Agilent Technologies, California, USA) using gDNA 165KB Analysis Kit (Cat No:FP-1002-0275).

The library was constructed using the SMRTbell Express template Preparation Kit 3.0 (Pacific Biosciences, California, USA) as per manufacturers’ protocol. The prepared library was purified using AMPure PB beads (Pacific Biosciences, California, USA). AMPure PB beads size selection carried to remove fragments shorter than 5 kb. Size selected SMRT libraries were purified and library bound complex was prepared using Sequel II binding kit. About 90 pM of the libraries was loaded on one SMRTcell containing 8M ZMW and sequenced in PacBio Sequel II system in CCS/HiFi mode. The prepared library was sequenced with a 30hr movie time. The generated subreads were converted to HiFi reads using Code Composure Studio (CCS) (version 6.3.0). The HiFi reads were used to create a primary assembly using hifiasm (version 0.19.2-r560).

Mitogenome extraction, annotation and visualization: Mitochondrial genome was identified and extracted from the primary assembly using mitoHiFi (v3.2.2)[26]. Mitogenome annotation was done using mitoZ (v3.6)[27]. Proksee (https://proksee.ca/) was used to annotate and visualize the assembled mitogenome.

Sequence analysis: Nucleotide composition and codon usage pattern (RSCU) were analysed using MEGA11[28] and strand asymmetry of the whole mitogenome was calculated based on the following formulas: AT skew=(A-T)/(A+T) and GC skew=(G-C)/(G+C)[29]. The secondary structure of each tRNA was predicted using tRNAscan-SE 2.0 web server[30]. The non-synonynous substitutions (Ka), synonymous substitutions (Ks) and their ratios (Ks/Ks) in the 13 mitochondrial Protein Coding Genes (PCGs) were calculated for the 27 whole mitogenome sequences of Bos grunniens available in public database and Arunachali mitochondrial genome using DnaSP version 6.12.03[31](Supplementary Table S1).

Sequence alignment and phylogenetic analysis: For phylogenetic study, 27 whole mitogenome sequence of different yak breeds of China were downloaded from NCBI database including one sequence of Bos indicus to be included as an outgroup (Supplementary Table S2) and with these, three datasets were generated to construct phylogenetic trees.

The first dataset (WMT), included whole mitogenomes of all the sequences which were aligned along with our sequence using the MUSCLE algorithm of MEGA11[23]. The best fit substitution model for alignment was determined as Tamura-Nei model using a discrete Gamma distribution (+G) with 5 rate categories (Supplementary Table S3). The aligned sequences were used for constructing the phylogeny tree using Maximum Likelihood (ML) method with 1000 bootstrap replications. For the remaining two datasets, each of the PCGs and control region for all the sequences were separately aligned and assessed using BioEdit version 7.7.1[32]. The alignments of the individual genes and control region were then concatenated in MEGA 11 software to generate the following two datasets: 1) 13PCGs-nucleotide sequences of the 13PCGs (11379bp) 2) DLOOP- nucleotide sequences of the D-loop or control region (916 bp). The corresponding best fit model substitution model for each of the dataset was determined using ModelFinder[33] function in IQ-TREE version 1.6.3[34] (Supplementary Table S4-S5) and the model with lowest Bayesian information criterion (BIC) was selected. The ML trees were constructed in IQ-TREE version 1.6.3 software and node confidence values were evaluated with 20,000 ultrafast bootstraps[35]. The phylogeny tree for all the three datasets were then visualised in iTOL version 6.9[36].

Mitogenome structure and organization: The Arunachali yak mitogenome had the distinctive characteristics of a mammalian mitochondrial genome. The mitogenome was a closed-circular double-stranded DNA molecule of 16,324 base pairs (bp) comprising 37 genes (13 protein coding genes (PCGs), 22 tRNAs, 2 rRNAs) and a non-coding control region (D-loop) (Table 1). The size of whole mitochondrial genome typically ranges from16,321 bp as in Meiren yak[37] to 16,325bp in Bazhou yak[38]. The gene order and arrangement were comparable to those of previously documented yak mitogenomes[39,40] and related bovid species[21,22].

Table 1: Gene content of Arunachali yak mitogenome

Group of genes	Name of genes
Protein coding genes (PCGs)	ND1, ND2, ND3, ND4, ND4L, ND5, ND6, COX1, COX2, COX3, Cytb, ATP6, ATP8
Ribosomal RNAs (rRNAs)	16s-rRNA (l-rRNA), 12s-rRNA (s-rRNA)
Transfer RNAs (tRNAs)	tRNA-Phe, tRNA-Val, tRNA-Leu, tRNA-Ile, tRNA-Gln, tRNA-Met, tRNA-Trp, tRNA-Ala, tRNA-Asn, tRNA-Cys, tRNA-Tyr, tRNA-Ser, tRNA-Asp, tRNA-Lys, tRNA-Gly, tRNA-Arg, tRNA-His, tRNA-Ser, tRNA-Leu, tRNA-Glu, tRNA-Thr, tRNA-Pro
Non-coding gene	Control region or D-loop

A total of 29 genes including 12 PCGs, 15 tRNAs, 2 rRNAs were encoded on the heavy (H) strand while the remaining PCG, ND6 and 7 tRNAs on the light (L) strand. Gene overlaps and intergenic or non-coding regions were also observed in the mitogenome1-40 bp (Table 2, Figure 1). There were 12 gene overlaps and the longest one involved 40bp between ATP8 and ATP6. The overlap between these two genes has been reported in other mitochondrial studies and appears to be a common occurrence[41]. Overall, 15 intergenic regions ranging from1-31 bp were identified. Aside from the D-loop region, the longest intergenic region occurred between trnN and trnC. This region of 31bp has been annotated in some studies as the origin for the replication of light (L) strand[42].

Nucleotide composition: The nucleotide composition of the whole mitogenome was found to be overall biased towards adenine and thymine with AT content at 60.98% and GC at 39.02% with each nucleotide content at A=33.70%, T=27.28%, G=13.21% and C=25.80%. The AT bianess is a typical characteristic of the mitochondrial genome among all the vertebrates [21-22,25,37-40]. The AT and GC content did not vary much among the different regions and greatest amount of AT was observed in the tRNA region while GC content was most significant in the PCGs. Additionally, the mitogenome had positive AT skew (0.11) and negative GC skew (0.32) which suggests higher content of adenosine and cytosine than their complementary nucleotides (Table 3).

Table 2: Mitochondrial genome annotation of Arunachali yak. H-heavy strand and L- light strand.

Gene Name	Start	End	Length (bp)	Strand	Anti-codon	Start codon	Stop codon	Space(+) / Overlap(-)
trnF	1	67	67	H	GAA			0
12s rRNA	68	1024	957	H				0
trnV	1025	1091	67	H	TAC			0
16s-rRNA	1090	2661	1572	H				-2
trnL	2663	2737	75	H	TAA			1
ND1	2740	3696	957	H		ATG	TAA	2
trnI	3696	3764	69	H	GAU			-1
trnQ	3762	3833	72	L	TTG			-3
trnM	3836	3904	69	H	CAT			2
ND2	3905	4948	1044	H		ATA	TAG	-1
trnW	4947	5013	67	H	TCA			-2
trnA	5015	5083	69	L	TGC			1
trnN	5085	5158	74	L	GTT			1
trnC	5191	5257	67	L	GCA			31
trnY	5258	5325	68	L	GTA			0
COX1	5327	6871	1545	H		ATG	TAA	1
trnS	6869	6937	69	L	TGA			-3
trnD	6945	7012	68	H	GTC			7
COX2	7014	7697	684	H		ATG	TAA	1
trnK	7701	7767	67	H	TTT			3
ATP8	7769	7969	201	H		ATG	TAA	1
ATP6	7930	8610	681	H		ATG	TAA	-40
COX3	8610	9390	781	H		ATG	T--	-1
trnG	9394	9462	69	H	TCC			3
ND3	9463	9819	357	H		ATA	TAG	0
trnR	9810	9878	69	H	TCG			-10
ND4L	9879	10175	297	H		ATG	TAA	0
ND4	10169	11546	1378	H		ATG	T--	-7
trnH	11547	11616	70	H	GTG			0
trnS	11617	11676	60	H	GCT			0
trnL	11678	11747	70	H	TAG			1
ND5	11748	13568	1821	H		ATA	TAA	0
ND6	13552	14079	528	L		ATG	TAA	-17
trnE	14080	14148	69	L	TTC			0
Cytb	14153	15292	1140	H		ATG	AGA	4
trnT	15296	15365	70	H	TGT			3
trnP	15365	15430	66	L	TGG			-1
D-loop	15431	16324	894	H				0

Table 3: Nucleotide composition of Arunachali yak mitogenome

Region	T%	C%	A%	G%	A+T	G+C	AT Skew	GC Skew
Whole genome	27.28	25.80	33.70	13.21	60.98	39.02	0.11	-0.32
PCGs	28.90	26.30	31.80	12.90	60.70	39.20	0.05	-0.34
tRNAs	30.29	19.34	32.13	18.23	62.42	37.58	0.03	-0.03
rRNAs	23.61	21.43	37.49	17.48	61.09	38.91	0.23	-0.10
D-loop	28.52	25.28	32.33	13.87	60.85	39.15	0.06	-0.29

PCGs and Codon Usage: The 13 PCGs of Arunachali yak mitogenome had a total length of 11379 bp coding 3793 amino acids which accounted for 69.71% of the total sequence. The initiation codon for all the PCGs were the typical ATN start codon. The start codon of most of the genes viz. ND1, COX1, COX2, COX3, ATP8, ATP6, ND4 ND4L, ND6, Cytb were ATG while three genes ND2, ND3 and ND5 used ATA codon for initiation of transcription. With respect to stop codon, eight out of the thirteen PCGs had TAA as their stop codon, COX3 and ND4 terminated with a single T residue which is also observed in other vertebrates [23,39] . The stop codon for ND2 and ND3 in Arunachali yak mitogenome was TAG while other mammalian mitogenome studies have reported the stop codon for ND3 gene as T-residue[23,37,42-43]. However, TAG as stop codon for mitochondrial genome was observed for an ancient cattle[44]. The Cytb gene used a unique stop codon AGA to terminate transcription[39-40, 43] (Table 2).

Table 4: Codon count and relative synonymous codon usage

Codon	Count	RSCU	Codon	Count	RSCU	Codon	Count	RSCU	Codon	Count	RSCU
UUU(F)	100	1.06	UCU(S)	106	1.2	UAU(Y)	177	1.27	UGU(C)	45	1
UUC(F)	88	0.94	UCC(S)	97	1.1	UAC(Y)	102	0.73	UGC(C)	45	1
UUA(L)	128	1.29	UCA(S)	106	1.2	UAA(*)	171	1.65	UGA(W)	54	1.15
UUG(L)	41	0.41	UCG(S)	37	0.42	UAG(*)	85	0.82	UGG(W)	40	0.85
CUU(L)	118	1.19	CCU(P)	145	1.39	CAU(H)	136	1.18	CGU(R)	31	0.89
CUC(L)	108	1.09	CCC(P)	130	1.25	CAC(H)	95	0.82	CGC(R)	38	1.09
CUA(L)	144	1.45	CCA(P)	104	1	CAA(Q)	156	1.43	CGA(R)	37	1.06
CUG(L)	58	0.58	CCG(P)	37	0.36	CAG(Q)	62	0.57	CGG(R)	33	0.95
AUU(I)	157	1.14	ACU(T)	162	1.43	AAU(N)	217	1.15	AGU(S)	80	0.9
AUC(I)	118	0.86	ACC(T)	113	1	AAC(N)	161	0.85	AGC(S)	105	1.19
AUA(M)	144	1.4	ACA(T)	135	1.19	AAA(K)	218	1.48	AGA(*)	74	0.71
AUG(M)	61	0.6	ACG(T)	44	0.39	AAG(K)	77	0.52	AGG(*)	85	0.82
GUU(V)	26	0.79	GCU(A)	61	1.23	GAU(D)	42	0.97	GGU(G)	31	1.16
GUC(V)	34	1.03	GCC(A)	63	1.27	GAC(D)	45	1.03	GGC(G)	23	0.86
GUA(V)	54	1.64	GCA(A)	64	1.29	GAA(E)	75	1.34	GGA(G)	31	1.16
GUG(V)	18	0.55	GCG(A)	10	0.2	GAG(E)	37	0.66	GGG(G)	22	0.82

The relative synonymous codon usage (RSCU) calculated for each amino acid (except for the stop codons) in the mitogenome indicated the most frequently used codon as Lys (AAA) followed by Asn (AAU), Tyr (UAU) and Thr (ACU) as the top five. The least commonly used codon was Ala (GCG) with only 10 counts (Table 4, Figure 2). The most abundant amino acids were Leucine, Serine, Threonine, Proline and Asparagine. In general, it was observed that the codons ending with A or T were more preferred than those with G or C in the third position when coding the same amino acid. This may be the cause of AT biasness in the whole mitogenome. Furthermore, the distribution pattern of the codons in each of the amino acid can act as marker for species level identification of animals[45].

The Ka, Ks and Ka/Ks ratio were calculated for each of the 13 PCGs (Figure 3) to estimate the selection pattern of these PCGs. It was observed that the Ka/Ks ratio was very low (less than 1.0) for all the genes and the ratio was 0 in four of the genes (Supplementary Table S1). There was absence of non-synonymous substitution in COX1, COX2 and ND1 genes while ND6 genes in the mitogenomes under study lacked synonymous substitution. Overall, it may be assumed that there is presence of purifying selection in these breeds and as such evolutionary stability is ensured[46-47]. Purifying selection is vital to prevent deleterious mutations from taking over a population and to ensure that any better structures are kept for as long as they can be maintained[48].

Transfer RNAs and ribosomal RNAs: The mitogenome of Arunachali yak consisted of 22 tRNAs with a total length of 1779 bp ranging from 60bp in trnS1 to 75bp in trnL (Table 2). The total AT content in tRNAs was 62.42% and that of GC was 37.58% (Table 3) suggesting AT biasness. All the tRNAs exhibited clover-leaf secondary structures except for Serine1 and Lysine which lacked D or dihydrouridine arm and loop respectively (Figure 4). Such structures have been defined in other domestic animals like Indian gaur[22], Indian wild pig[23], Camels[24]and closely related species Indian Mithun[21].The 12s and 16s rRNA genes of Arunachali yak were of 957bp and 1572bp respectively in lengths. 12s rRNA was located between trnF and trnV genes and 16s rRNA was annotated between trnV and trnL. The two rRNA genes had an AT content of 61.09 % making these an AT-rich region.

D-loop or control region: D-loop or the control region in the mitogenome was located between trnP and trnF and had an A+T content of 60.85%. The region was found to be 894 bp in length which is akin to the length of D-loop reported in other yak breeds [49-50]. As inferred from other studies, the length of D-loop usually ranges from 891 bp[36] to 895 bp[43]. The mitogenome of Arunachali yak also showed the presence multiple copies of palindromic motifs ‘ATGTA’ and ‘TACAT’, however not in pairs as documented for Sichuan takin or Tibetan takin [25]. These short sequences are hypothesised to be sites for termination of H-strand elongation during replication process[22]. The control region terminates with the characteristic homo-polymeric C stretch of 13bp as also observed in other bovids[21-22,43,51-52] (Figure S1).

Phylogenetic analysis: Maximum likelihood method with different best fit substitution models were used for establishing the phylogenetic relationship among the Bos grunniens sequences included in this study. A total of three phylogenetic trees (WMT, 13PCGs and DLOOP) were constructed using three datasets as shown in Figure 5. In all the three trees, our sequence of Arunachali yak clusters consistently with ten of the Chinese yak breeds viz. Sibu, Bazhou, Seron, Jinchuan, Zhongdian, Tongde, Pali, Meiren, Leiwuqi and Gaoshan. The phylogenetic tree of concatenated mitochondrial PCGs (13PCGs) is comparable to the percent sequence identity of the sequences[53] (Supplementary Table S6) with more similar sequences clustering in the same clade. This tree is also in consensus with other studies on yak mitochondrial genome[43,51]. Therefore, concatenated PCGs may be a better dataset for construction of phylogenetic tree in case of mitogenome. The DLOOP tree shows Arunachali yak to be closely related to Jinchuan yak. The D-loop or control region has the highest variability in the whole of mitogenome and has been proven to be powerful marker for study of maternal phylogenetic and evolutionary relationships among breeds[23]. It may therefore be hypothesised that Arunachali yak and Jinchuan yak have the closest relation and shared the same ancestor before domestication.

This study has reported the first ever complete mitogenome of Indian yak (Arunachali) which is a unique livestock germplasm of the trans-Himalayan region with immense socio-economic and cultural significance to the transhumant pastoralist, Brokpas. The mitogenome sequence, gene arrangement and organization were found to be highly conserved with other yak breeds as well as mammals. The mitogenomic features like base composition, codon usage and phylogenetic relationship with Chinese yak breeds were also analysed. Phylogenetic analysis revealed common ancestry of Indian yak with other yak breeds with close relation to the Jinchuan breed of yak in terms of the conservation of their D-loop region. The results of this study may thus provide ground for characterisation of yak breeds found in other regions of India and also for further genomic studies in Poephagus grunniens.

Acknowledgements

This study is funded by DBT, India under NEH-Programme sanction order no.: DBT/PR44955/NER/95/1883/2021 dated 21/02/2023. Authors are thankful to Indian Council of Agricultural Research for providing necessary facilities required for this study. The authors also acknowledge the technical support of Nucleome Informatics Pvt.Ltd., Hyderabad, India.

Author contributions

M.P., M.S and P.J.D. conceptualised the work. M.P. secured the grant, collected the sample and wrote the manuscript. M.P. and K.U.T analysed the data and prepared figures and tables.

Data availability statement

The assembled mitochondrial genome sequence is available in GenBank of NCBI under Accession no. PP744587 (Submitted on 01.05.2024).

Additional Information

Supplementary information

Provided as Supplementary Table S1-S7 and Supplementary Figure S1.

Competing Interests Statement

The authors declare no competing interests.

Ethical Statements

The collection of sample was with the approval of the Committee for Control and Supervision of Experiments on Animals (CCSEA), New Delhi, India vide office order no. V-11011(13)/13/2022-CPCSEA-DADF dated 06.01.2023.

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No competing interests reported.

Complete mitogenome structure and phylogenetic implications of the first Indian yak breed- Arunachali (Poephagus grunniens L.)

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Version 1

Abstract

Introduction

Materials and methods

Results and Discussion

Conclusion

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1