Abstract
The genus Ammopiptanthus is mainly distributed in the semi-arid regions of northwest China. It only contains two species: A. mongolicus and A. nanus. They exhibit similar morphological characteristics, but little is known about their genetic differences. We performed de novo sequencing and mitochondrial genome assembly and found that both species contain 36 protein-coding genes, 3 rRNA, and 16 tRNA genes. The comparison of A. mongolicus and A. nanus mitogenomes revealed a 6.5-kb region loss in A. nanus mitogenome, which was replaced by a 1.5-kb different sequence element. Other small variations between the two species include 25 SNPs, 4 deletions, and 2 insertions. Meta-analyses indicated that 34% of the A. mongolicus mitogenome was unique to Ammopiptanthus and has no similarity with any other known legume mitogenomes. These unique sequences are mainly distributed in intergenic regions. Gene gain and loss analysis showed that this mitogenome gained two genes, rps7 and sdh4, during evolution, with rps7 transferred from the chloroplast genome. Selective pressure analysis implied that the atp8 gene was under positive selection. Our study established high-quality reference mitogenomes for the genus Ammopiptanthus, revealed novel genetic differences between A. mongolicus and A. nanus, and provided new insights into the evolution of legume plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams KL, Palmer JD (2003) Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. J Molec Evol 29:380–395. https://doi.org/10.1016/S1055-7903(03)00194-5
Aljohi HA, Liu W, Lin Q, Zhao Y, Zeng J, Alamer A, Alanazi LO, Alawad AO, Al-Sadi AM, Hu S, Yu J (2016) Complete sequence and analysis of coconut palm (Cocos nucifera) mitochondrial genome. PLoS ONE 11:e0163990. https://doi.org/10.1371/journal.pone.0163990
Alverson AJ, Rice DW, Dickinson S, Barry K, Palmer JD (2011a) Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Pl Cell 23:2499–2513. https://doi.org/10.1105/tpc.111.087189
Alverson AJ, Zhuo S, Rice DW, Sloan DB, Palmer JD (2011b) The mitochondrial genome of the legume Vigna radiata and the analysis of recombination across short mitochondrial repeats. PLoS ONE 6:e16404. https://doi.org/10.1371/journal.pone.0016404
Assefa S, Keane TM, Otto TD, Newbold C, Berriman M (2009) ABACAS: algorithm-based automatic contiguation of assembled sequences. Bioinformatics 25:1968–1969. https://doi.org/10.1093/bioinformatics/btp347
Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucl Acids Res 27:573–580. https://doi.org/10.1093/nar/27.2.573
Berlin K, Koren S, Chin CS, Drake JP, Landolin JM, Phillippy AM (2015) Assembling large genomes with single-molecule sequencing and locality-sensitive hashing. Nat Biotechnol 33:623–630. https://doi.org/10.1038/nbt.3238
Bi C, Paterson AH, Wang X, Xu Y, Wu D, Qu Y, Jiang A, Ye Q, Ye N (2016) Analysis of the complete mitochondrial genome sequence of the diploid cotton Gossypium raimondii by comparative genomics approaches. Biomed Res Int 2016:5040598. https://doi.org/10.1155/2016/5040598
Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W (2010) Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27:578–579. https://doi.org/10.1093/bioinformatics/btq683
Chaisson MJ, Tesler G (2012) Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): application and theory. BMC Bioinform 13:238. https://doi.org/10.1186/1471-2105-13-238
Chang S, Wang Y, Lu J, Gai J, Li J, Chu P, Guan R (2013) The mitochondrial genome of soybean reveals complex genome structures and gene evolution at intercellular and phylogenetic levels. PLoS ONE 8:e56502. https://doi.org/10.1371/journal.pone.0056502
Cheng SH (1959) Ammopiptanthus Cheng f. A new genus of Leguminosae from central Asia. J Bot USSR 44:1381–1386 (in Russian)
Chevreux B, Wetter T, Suhai S (1999) Genome sequence assembly using trace signals and additional sequence information. In: Proceedings of the German Conference on Bioinformatics, GCB '99, October 4-6, 1999, Hannover, Germany, pp 45–56
Chitra L, Boopathy R (2013) Adaptability to hypobaric hypoxia is facilitated through mitochondrial bioenergetics: an in vivo study. Brit J Pharmacol 169:1035–1047. https://doi.org/10.1111/bph.12179
Cronk Q, Ojeda I, Pennington RT (2006) Legume comparative genomics: progress in phylogenetics and phylogenomics. Curr Opin Pl Biol 9:99–103. https://doi.org/10.1016/j.pbi.2006.01.011
English AC, Richards S, Han Y, Wang M, Vee V, Qu JX, Qin X, Muzny DM, Reid JG, Worly KC, Gibbs RA (2012) Mind the gap: upgrading genomes with Pacific Biosciences RS long-read sequencing technology. PLoS ONE 7:e47768. https://doi.org/10.1371/journal.pone.0047768
Feng L, Gu LF, Luo J, Fu AS, Ding Q, Yiu SM, He JX (2017) Complete plastid genomes of the genus Ammopiptanthus and identification of a novel 23-kb rearrangement. Conservation Genet Resources 9:647–650. https://doi.org/10.1007/s12686-017-0747-8
Gao F, Wang JY, Wei SJ, Li ZL, Wang N, Li HY, Feng JC, Li HJ, Zhou YJ (2015) Transcriptomic analysis of drought stress responses in Ammopiptanthus mongolicus leaves using the RNA-Seq technique. PLoS ONE 10:e0124382. https://doi.org/10.1371/journal.pone.0124382
Gao F, Wang N, Li HY, Li JS, Fu CX, Xiao ZH, Wei CX, Lu XD, Feng JC, Zhou YJ (2016) Identification of drought-responsive microRNAs and their targets in Ammopiptanthus mongolicus by using high-throughput sequencing. Sci Rep 6:34601. https://doi.org/10.1038/srep34601
Gao F, Li HY, Xiao ZH, Wei CX, Feng JC, Zhou YJ (2017) De novo transcriptome analysis of Ammopiptanthus nanus and its comparative analysis with A. mongolicus. Trees 32:287–300. https://doi.org/10.1007/s00468-017-1631-6
Gao F, Wang X, Li XM, Xu MY, Li HY, Abla M, Sun HG, Wei SJ, Feng JC, Zhuo YJ (2018) Long-read sequencing and de novo genome assembly of Ammopiptanthus nanus, a desert shrub. GigaScience 7:giy074. https://doi.org/10.1093/gigascience/giy074
Ge XJ, Yu Y, Yuan YM, Huang HW, Yan C (2005) Genetic diversity and geographic differentiation in endangered Ammopiptanthus (Leguminosae) populations in desert regions of northwest China as revealed by ISSR analysis. Ann Bot (Oxford) 95:843–851. https://doi.org/10.1093/aob/mci089
Han SH, Li JS (1992) Characteristics of leaf structure of Ammopiptanthus mongolicus and its relation with cold resistance. Sci Silvae Sin 28:198–201 (in Chinese)
He JX, Wang Y, Fu JR (1996) An improved CTAB method for extraction of DNA from recalcitrant seeds. Pl Physiol Commun 32:208–210 (in Chinese)
Jeffares DC, Tomiczek B, Sojo V, dos Reis M (2015) A beginners guide to estimating the non-synonymous to synonymous rate ratio of all protein-coding genes in a genome. Meth Molec Biol 1201:65–90. https://doi.org/10.1007/978-1-4939-1438-8_4
Jiang ZR (2000) Probe into drought-resisting mechanism of Ammopiptanthus mongolicus (Maxim.) Cheng F. J Desert Res 20:71–74. https://doi.org/10.3321/j.issn:1000-694X.2000.01.015 (in Chinese)
Krumsiek J, Arnold R, Rattei T (2007) Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 23:1026–1028. https://doi.org/10.1093/bioinformatics/btm039
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra M (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645. https://doi.org/10.1101/gr.092759.109
Kubo T, Newton KJ (2008) Angiosperm mitochondrial genomes and mutations. Mitochondrion 8:5–14. https://doi.org/10.1016/j.mito.2007.10.006
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis Version 7.0 for bigger datasets. Molec Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nature Meth 9:357–359. https://doi.org/10.1038/nmeth.1923
Lei W, Ni D, Wang Y, Shao J, Wang X, Yang D, Wang J (2016) Intraspecific and heteroplasmic variations, gene losses and inversions in the chloroplast genome of Astragalus membranaceus. Sci Rep 6:21669. https://doi.org/10.1038/srep21669
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Liu S, Ni Y, He Q, Wang J, Chen Y, Lu C (2017) Genome-wide identification of microRNAs that respond to drought stress in seedlings of tertiary relict Ammopiptanthus Mongolicus. Hort Pl J 3:209–218. https://doi.org/10.1016/j.hpj.2017.10.003
Lohse M, Drechsel O, Kahlau S, Bock R (2013) OrganellarGenomeDRAW—a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucl Acids Res 41:575–581. https://doi.org/10.1093/nar/gkt289
Lowe TM, Chan PP (2016) tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucl Acids Res 44:54–57. https://doi.org/10.1093/nar/gkw413
Martin W (2003) Gene transfer from organelles to the nucleus: frequent and in big chunks. Proc Natl Acad Sci USA 100:8612–8614. https://doi.org/10.1073/pnas.1633606100
Martin GE, Rousseau-Gueutin M, Cordonnier S, Lima O, Michon-Coudouel S, Naquin D, Carvalho JF, Aïnouche M, Salmon A, Aïnouche A (2014) The first complete chloroplast genome of the Genistoid legume Lupinus luteus: evidence for a novel major lineage-specific rearrangement and new insights regarding plastome evolution in the legume family. Ann Bot (Oxford) 113:1197–1210. https://doi.org/10.1093/aob/mcu050
Ogihara Y, Yamazaki Y, Murai K, Kanno A, Terachi T, Shiina T, Miyashita N, Nashuda S, Nakamura C, Mori N, Takumi S, Murata M, Futo S, Tsunewaki K (2005) Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome. Nucl Acids Res 33:6235–6250. https://doi.org/10.1093/nar/gki925
Pang T, Ye CY, Xia XL, Yin WL (2013) De novo sequencing and transcriptome analysis of the desert shrub, Ammopiptanthus mongolicus, during cold acclimation using Illumina/Solexa. BMC Genom 14:488. https://doi.org/10.1186/1471-2164-14-488
Pang T, Guo LL, Shim D, Cannon N, Tang S, Chen JH, Xia XL, Yin WL (2015) Characterization of the transcriptome of the xerophyte Ammopiptanthus mongolicus leaves under drought stress by 454 pyrosequencing. PLoS ONE 10:e0136495. https://doi.org/10.1371/journal.pone.0136495
Quinlan AR (2014) BEDTools: the Swiss-Army tool for genome feature analysis. Curr Protoc Bioinf 47:1–34. https://doi.org/10.1002/0471250953.bi1112s47
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molec Phylogen Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Shi J, Liu MQ, Chen YZ, Wang JY, Lu CF (2016) Heterologous expression of the dehydrin-like protein gene AmCIP from Ammopiptanthus mongolicus enhances viability of Escherichia coli and tobacco under cold stress. Pl Growth Regulat 79:71–80. https://doi.org/10.1007/s10725-015-0112-4
Shi W, Liu PL, Duan L, Pan BR, Su ZH (2017) Evolutionary response to the Qinghai-Tibetan Plateau uplift: phylogeny and biogeography of Ammopiptanthus and tribe Thermopsideae (Fabaceae). PeerJ 5:e3607. https://doi.org/10.7717/peerj.3607
Su ZH, Pan BR, Zhang ML, Shi W (2016) Conservation genetics and geographic patterns of genetic variation of endangered shrub Ammopiptanthus (Fabaceae) in northwestern China. Conservation Genet 17:485–496. https://doi.org/10.1007/s10592-015-0798-x
Thiel T, Michalek W, Varshney R, Graner A (2003) Exploiting EST databases for the development and characterization of genederived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106:411–422. https://doi.org/10.1007/s00122-002-1031-0
Tucker SC (2003) Floral development in legumes. Pl Physiol 131:911–926. https://doi.org/10.1104/pp.102.017459
Vembar SS, Seetin M, Lambert C, Nattestad M, Schatz MC, Baybayan P, Scherf A, Smith ML (2016) Complete telomere-to-telomere de novo assembly of the Plasmodium falciparum genome through long-read (> 11 kb), single molecule, real-time sequencing. DNA Res 23:339–351. https://doi.org/10.1093/dnares/dsw022
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wartman J, Young SK, Earl AM (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9:e112963. https://doi.org/10.1371/journal.pone.0112963
Wang HC, Sun H (2001) A preliminary study on phytogeography of the tribe Thermopsideae (Papilionaceae). Acta Bot Yunnan 23:17–28. https://doi.org/10.3969/j.issn.2095-0845.2001.01.002 (in Chinese)
Wang HC, Sun H, Compton JA, Yang JB (2006) A phylogeny of Thermopsideae (Leguminosae: Papilionoideae) inferred from nuclear ribosomal internal transcribed spacer (ITS) sequences. Bot J Linn Soc 151:365–373. https://doi.org/10.1111/j.1095-8339.2006.00512.x
Wang YH, Wicke S, Wang H, Jin JJ, Chen SY, Zhang SD, Li DZ, Yi TS (2018) Plastid genome evolution in the early-diverging legume subfamily Cercidoideae (Fabaceae). Frontiers Pl Sci 9:138. https://doi.org/10.3389/fpls.2018.00138
Wei Z, Lock J (2010) Tribe Thermopsideae. Flora of China 10:100–104
Wu YQ, Wei W, Pang XY, Wang XF, Zhang HL, Dong B, Xing YP, Li XG, Wang M (2014) Comparative transcriptome profiling of a desert evergreen shrub, Ammopiptanthus mongolicus, in response to drought and cold stresses. BMC Genom 15:671. https://doi.org/10.1186/1471-2164-15-671
Xie L, Yang Y (2012) Miocene origin of the characteristic broad-leaved evergreen shrub Ammopiptanthus (Leguminosae) in the Desert Flora of Eastern Central Asia. Int J Pl Sci 173:944–955. https://doi.org/10.1086/667232
Xu MJ, Wang JH, Bu XL, Yu HL, Li P, Ou HY, He Y, Xu FD, Hu XY, Zhu XM, Ao P, Xu J (2016) Deciphering the streaml-ined genome of Streptomyces xiamenensis 318 as the producer of the anti-fibrotic drug candidate xiamenmycin. Sci Rep 6:18977. https://doi.org/10.1038/srep18977
Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Computer Applic Biosci 13:555–556. https://doi.org/10.1093/bioinformatics/13.5.555
Ye N, Wang X, Li J, Bi C, Xu Y, Wu D, Ye Q (2017) Assembly and comparative analysis of complete mitochondrial genome sequence of an economic plant Salix suchowensis. PeerJ 5:e3148. https://doi.org/10.7717/peerj.3148
Yu HQ, Zhou XY, Wang YG, Zhou SF, Fu FL, Li WC (2017) A betaine aldehyde dehydrogenase gene from Ammopiptanthus nanus enhances tolerance of Arabidopsis to high salt and drought stresses. Pl Growth Regulat 2:265–276. https://doi.org/10.1007/s10725-016-0245-0
Yu TQ, Sun LC, Cui HW, Liu SL, Men JY, Chen SL, ChenYZ LuCF (2018) The complete mitochondrial genome of a tertiary relict evergreen woody plant Ammopiptanthus mongolicus. Mitochondrial DNA B Resources 3:9–11. https://doi.org/10.1080/23802359.2017.1413301
Zhang T, Fang Y, Wang X, Deng X, Zhang X, Hu S, Yu J (2012) The complete chloroplast and mitochondrial genome sequences of Boea hygrometrica: insights into the evolution of plant organellar genomes. PLoS ONE 7:e30531. https://doi.org/10.1371/journal.pone.0030531
Zhou YJ, Gao F, Liu R, Feng JC, Li HJ (2012) De novo sequencing and analysis of root transcriptome using 454 pyrosequencing to discover putative genes associated with drought tolerance in Ammopiptanthus mongolicus. BMC Genom 13:266. https://doi.org/10.1186/1471-2164-13-266
Acknowledgements
This work was supported by the National Natural Science Foundation of China (NSFC) (No. 91125027), the GRF grants (14121915, 14148916) and AoE grants (AoE/M-05/12, AoE/M-403/16) from the Research Grant Council (RGC) of Hong Kong, the grant from the NSFC-RGC Joint Scheme (N_CUHK452/17), National Key Research and Development Program—Key Innovative and Collaborative Science and Technology Scheme for Hong Kong, Macau, and Taiwan (Grant 2017YFE0191100), the Shenzhen Science & Technology Research & Development Funding—Peacock Scheme, and the Direct Grants from The Chinese University of Hong Kong. We thank Minqin Eremophytes Botanical Garden (Minqin County, Gansu Province) for providing A. mongolicus seeds and Mr. Zhiyuan Li for technical help. We also thank Ms. Yue Qin and Ms. Chen Huang for their help in writing the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Eric Schranz.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Information on Electronic Supplementary Material
Information on Electronic Supplementary Material
Online Resource 1. Detailed parameters of programs used in this study.
Online Resource 2. The length distribution of long reads used for Ammopiptanthus mongolicus mitogenome assembly.
Online Resource 3. DNA sequence alignment of the rps7 gene in mitogenome and plastome of Ammopiptanthus mongolicus.
Online Resource 4. SSRs in the mitogenome of Ammopiptanthus mongolicus.
Online Resource 5. DNA sequence alignment of the rps3 gene in Ammopiptanthus mongolicus (AM) and A. nanus (AN).
Online Resource 6. Dot matrix plots showing the comparison of our assembly results to sequence from a previous study.
Online Resource 7. Distribution of disperse repeats (> 100 bp) in mitogenome of Ammopiptanthus mongolicus.
Online Resource 8. Protein Sequence alignment of atp8 gene from mitogenomes of legumes.
Rights and permissions
About this article
Cite this article
Feng, L., Li, N., Yang, W. et al. Analyses of mitochondrial genomes of the genus Ammopiptanthus provide new insights into the evolution of legume plants. Plant Syst Evol 305, 385–399 (2019). https://doi.org/10.1007/s00606-019-01578-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00606-019-01578-2