The Genetic and Environmental Adaptation of the Associated Liana Species Derris trifoliata Lour. (Leguminosae) in Mangroves
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials and DNA Extraction
2.2. SLAF Library Construction and High-Throughput Sequencing
2.3. SLAF-seq Data Grouping and SNPs Discovery
2.4. Phylogenetic Analysis
2.5. Genetic Analysis
2.6. Association Analyses between SNPs and Environmental Factors
3. Results
3.1. Sequence and Quality Statistics Based on SLAF-seq
3.2. Phylogenetic Analysis
3.3. Genetic Diversity
3.4. Clonal Diversity and Clonal Structure
3.5. Associations between SNP Markers and Environmental Variables
4. Discussion
4.1. Phylogenetic Analysis
4.2. Genetic Diversity
4.3. Clonal Diversity and Clonal Structure
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Wicaksono, P.; Hartono, D.P.; Nehren, U. Mangrove biomass carbon stock mapping of the Karimunjawa Islands using multispectral remote sensing. Int. J. Remote Sens. 2016, 37, 26–52. [Google Scholar] [CrossRef]
- Collins, D.S.; Avdis, A.; Allison, P.A.; Johnson, H.D.; Hill, J.; Piggott, M.D.; Hassan, M.H.A.; Damit, A.R. Tidal dynamics and mangrove carbon sequestration during the Oligo–Miocene in the South China Sea. Nat. Commun. 2017, 15, 15698. [Google Scholar] [CrossRef]
- Xiong, Y.; Liao, B.; Wang, F. Mangrove vegetation enhances soil carbon storage primarily through in situ inputs rather than increasing allochthonous sediments. Mar. Pollut. Bull. 2018, 131, 378–385. [Google Scholar] [CrossRef]
- Badola, R.; Hussain, S.A. Valuing ecosystem functions: An empirical study on the storm protection function of Bhitarkanika mangrove ecosystem, India. Environ. Conserv. 2005, 32, 85–92. [Google Scholar] [CrossRef]
- Bell, J.; Lovelock, C.E. Insuring Mangrove Forests for Their Role in Mitigating Coastal Erosion and Storm-Surge: An Australian Case Study. Wetlands 2013, 33, 279–289. [Google Scholar] [CrossRef]
- Akber, M.A.; Patwary, M.M.; Islam, M.A.; Rahman, M.R. Storm protection service of the Sundarbans mangrove forest, Bangladesh. Nat. Hazards 2018, 94, 405–418. [Google Scholar] [CrossRef]
- Meziane, T.; Tsuchiya, M. Organic matter in a subtropical mangrove-estuary subjected to wastewater discharge: Origin and utilisation by two macrozoobenthic species. J. Sea Res. 2010, 47, 1–11. [Google Scholar] [CrossRef]
- Hoque, M.M.; Kamal, A.H.M.; Idris, M.H.; Ahmed, O.H.; Saifullah, A.S.M.; Billah, M.M. Status of some fishery resources in a tropical mangrove estuary of Sarawak, Malaysia. Mar. Biol. Res. 2015, 11, 834–846. [Google Scholar] [CrossRef]
- Xin, K.; Xie, Z.; Zhong, C.; Sheng, N.; Gao, C.; Xiao, X. Damage Caused by Sphaeroma to Mangrove Forests in Hainan, Dongzhaigang, China. J. Coast. Res. 2020, 36, 1197–1203. [Google Scholar] [CrossRef]
- Feng, J.; Zhou, J.; Wang, L.; Cui, X.; Ning, C.; Wu, H.; Zhu, X.; Lin, G. Effects of short-term invasion of Spartina alterniflora and the subsequent restoration of native mangroves on the soil organic carbon, nitrogen and phosphorus stock. Chemosphere 2017, 184, 774–783. [Google Scholar] [CrossRef]
- Schnitzer, S.A. A mechanistic explanation for global patterns of liana abundance and distribution. Am. Nat. 2005, 166, 262–276. [Google Scholar] [CrossRef] [Green Version]
- Schnitzer, S.A.; Bongers, F. Increasing liana abundance and biomass in tropical forests: Emerging patterns and putative mechanisms. Ecol. Lett. 2011, 14, 397–406. [Google Scholar] [CrossRef] [Green Version]
- Wu, B.; Geng, S.L.; Shu, B. Genetic variation and the conservation of isolated populations of Derris trifoliata (Leguminosae), a mangrove-associated vine, in southern China. Biochem. Syst. Ecol. 2012, 40, 118–125. [Google Scholar] [CrossRef]
- Raju, A.J.S.; Kumar, R. Pollination ecology of Derris trifoliata (Fabaceae), a mangrove associate in Coringa Mangrove Forest, Andhra Pradesh, India. J. Threat. Taxa 2016, 8, 8788–8796. [Google Scholar] [CrossRef]
- Aluri, J.S.R.; Kumar, R.; Chappidi, P.R. Reproductive biology of mangrove plants clerodendrum inerme, Derris trifoliata, Suaeda maritima, Suaeda monoica, Suaeda nudiflora. Transylv. Rev. Syst. Ecol. Res. 2016, 18, 31–68. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Liao, B.; Xin, K.; Sheng, N. Allometric equations for liana species Derris trifoliata and the relationship between inflorescence generation and stem diameter. Glob. Ecol. Conserv. 2017, 26, e01511. [Google Scholar] [CrossRef]
- Stuefer, J.F.; Erschbamer, B.; Huber, H.; Suzuki, J. Ecology and Evolutionary Biology of Clonal Plants. Evol. Ecol. 2002, 15, 223–230. [Google Scholar] [CrossRef]
- Callaghan, T.V.; Svensson, B.M.; Bowman, H.; Lindley, D.K.; Carlssom, B.A. Models of clonal plant-growth based on population-dynamics and architecture. Oikos 1990, 57, 257–269. [Google Scholar] [CrossRef]
- Dering, M.; Chybicki, I.J.; Rączka, G. Clonality as a driver of spatial genetic structure in populations of clonal tree species. J. Plant Res. 2015, 128, 731–745. [Google Scholar] [CrossRef] [PubMed]
- Ley, A.C.; Hardy, O.J. Spatially limited clonality and pollen and seed dispersal in a characteristic climber of Central African rain forests: Haumania danckelmaniana (Marantaceae). Biotropica 2016, 48, 618–627. [Google Scholar] [CrossRef]
- Loh, R.; Scarano, F.R.; Alves-erreira, M.; Salgueiro, F. Clonality strongly affects the spatial genetic structure of the nurse species Aechmea nudicaulis (L.) Griseb. (Bromeliaceae). Bot. J. Linn. Soc. 2015, 178, 329–341. [Google Scholar] [CrossRef] [Green Version]
- Ren, M.X.; Zhang, Q.G. Clonal diversity and structure of the invasive aquatic plant Eichhornia crassipes in China. Aquat. Bot. 2007, 87, 242–246. [Google Scholar] [CrossRef]
- de Witte, L.C.; Armbruster, G.F.J.; Gielly, L.; Taberlet, P.; Stöcklin, J. AFLP markers reveal high clonal diversity and extreme longevity in four key arctic-alpine species. Mol. Ecol. 2012, 21, 1081–1097. [Google Scholar] [CrossRef]
- Yang, Y.J.; Ji-Ning, L.I.; Gong, L.; Zhou, J. Clonal Structure and Genetic Diversity of Natural var.Assessed by ISSR. Plant Sci. J. 2013, 31, 85–92. [Google Scholar] [CrossRef]
- Chenault, N.; Arnaud-Haond, S.; Juteau, M.; Valade, R.; Almeida, J.L.; Villar, M.; Bastien, C.; Dowkiw, A. SSR-based analysis of clonality, spatial genetic structure and introgression from the Lombardy poplar into a natural population of Populus nigra L. along the Loire River. Tree Genet. Genomes 2011, 7, 1249–1262. [Google Scholar] [CrossRef] [Green Version]
- Sun, X.; Liu, D.; Zhang, X.; Li, W.; Liu, H.; Hong, W.; Jiang, C.; Guan, N.; Ma, C.; Zeng, H. SLAF-seq: An Efficient Method of Large-Scale De Novo SNP Discovery and Genotyping Using High-Throughput Sequencing. PLoS ONE 2013, 8, e58700. [Google Scholar] [CrossRef]
- Gong, D.; Huang, L.; Xu, X.; Wang, C.; Ren, M.; Wang, C.; Chen, M. Construction of a high-density SNP genetic map in flue-cured tobacco based on SLAF-seq. Mol. Breed. 2016, 36, 1–12. [Google Scholar] [CrossRef]
- Duchoslavová, J.; Herben, T. Effect of clonal growth form on the relative performance of species in experimental communities over time. Perspect. Plant Ecol. Evol. Syst. 2020, 44, 125532. [Google Scholar] [CrossRef]
- Yu, H.W.; Wang, L.G.; Liu, C.H.; Yu, D.; Qu, J.H. Effects of a spatially heterogeneous nutrient distribution on the growth of clonal wetland plants. BMC Ecol. 2020, 20, 59. [Google Scholar] [CrossRef]
- Yorke, S.R.; Schnitzer, S.A.; Mascaro, J.; Letcher, S.G.; Carson, W.P. Increasing Liana Abundance and Basal Area in a Tropical Forest: The Contribution of Long-distance Clonal Colonization. Biotropica 2013, 45, 317–324. [Google Scholar] [CrossRef] [Green Version]
- Ledo, A.; Schnitzer, S.A. Disturbance and clonal reproduction determine liana distribution and maintain liana diversity in a tropical forest. Ecology 2014, 95, 2169–2178. [Google Scholar] [CrossRef]
- Pluess, A.R.; Stöcklin, J. Population genetic diversity of the clonal plant Geum reptans (Rosaceae) in the Swiss Alps. Am. J. Bot. 2004, 91, 2013–2021. [Google Scholar] [CrossRef]
- Solé, M.; Durka, W.; Eber, S.; Brandl, R. Genotypic and Genetic Diversity of the Common WeedCirsium arvense (Asteraceae). Int. J. Plant Sci. 2004, 165, 437–444. [Google Scholar] [CrossRef] [Green Version]
- Namroud, M.C.; Park, A.; Tremblay, F.; Bergeron, Y. Clonal and spatial genetic structures of aspen (Populus tremuloides Michx.). Mol. Ecol. 2005, 14, 2969–2980. [Google Scholar] [CrossRef]
- Zhang, Y.; Xin, K.; Liao, B.W.; Sheng, N.; Ai, X.H. The characteristics of pods and seeds of liana species Derris trifoliata and their relationship with environmental factors in Guangdong, China. Ecol. Indic. 2021, 129, 107930. [Google Scholar] [CrossRef]
- Gill, K.S.; Lubbers, E.L.; Gill, B.S.; Raupp, W.J.; Cox, T.S. A genetic linkage map of Triticum tauschii (DD) and its relationship to the D genome of bread wheat (AABBDD). Genome 1991, 34, 362–374. [Google Scholar] [CrossRef]
- Kozich, J.J.; Westcott, S.L.; Baxter, N.T.; Highlander, S.K.; Schloss, P.D. Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform. Appl. Environ. Microbiol. 2018, 79, 5112–5120. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, R.; Yu, C.; Li, Y.; Lam, T.-W.; Yiu, S.-M.; Kristiansen, K.; Wang, J. SOAP2, An improved ultrafast tool for short read alignment. Bioinformatics 2009, 25, 1966–1967. [Google Scholar] [CrossRef] [Green Version]
- Li, H.; Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25, 1754–1760. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McKenna, A.; Hanna, M.; Banks, E.; Sivachenko, A.; Cibulskis, K.; Kernytsky, A.; Garimella, K.; Altshuler, D.; Gabriel, S.; Daly, M.; et al. The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010, 20, 1297–1303. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; Durbin, R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25, 2078–2079. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Stecher, G.; Michael, L.; Knyaz, C.; Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef] [PubMed]
- Eickmeyer, K.; Huggins, P.; Pachter, L. On the optimality of the neighbor-joining algorithm. Algorithms Mol. Biol. 2008, 3, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Price, A.L.; Patterson, N.J.; Plenge, R.M.; Weinblatt, M.E.; Shadick, N.A.; Reich, D. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 2006, 38, 904–909. [Google Scholar] [CrossRef] [PubMed]
- Alexander, D.H.; Novembre, J.; Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009, 19, 1655–1664. [Google Scholar] [CrossRef] [Green Version]
- Ellstrand, N.C.; Roose, M.L. Patterns of Genotypic Diversity in Clonal Plant Species. Am. J. Bot. 1987, 74, 123–131. [Google Scholar] [CrossRef]
- Parker, K.C.; Hamrick, J.L. Genetic diversity and clonal structure in a columnar cactus, Lophocereus schottii. Am. J. Bot. 1992, 79, 86–96. [Google Scholar] [CrossRef]
- Peakall, R.; Smouse, P.E. GenAlEx 6.5, Genetic analysis in Excel. Population genetic software for teaching and research—An update. Bioinformatics 2012, 28, 2537–2539. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Foll, M.; Gaggiotti, O. A Genome-Scan Method to Identify Selected Loci Appropriate for Both Dominant and Codominant Markers: A Bayesian Perspective. Genetics 2008, 180, 977–993. [Google Scholar] [CrossRef] [Green Version]
- Eric, F.; Schoville, S.D.; Guillaume, B.; Olivier, F. Testing for Associations between Loci and Environmental Gradients Using Latent Factor Mixed Models. Mol. Biol. Evol. 2013, 30, 1687–1699. [Google Scholar]
- Altschul, S.F.; Madden, T.L.; Schffer, A.A.; Zhang, J.; Zhang, Z.; Webb, M.; Lipman, D.J. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997, 25, 3389–3402. [Google Scholar] [CrossRef] [Green Version]
- Ashburner, M.; Ball, C.A.; Blake, J.A.; Botstein, D.; Butler, H.; Cherry, J.M. Gene ontology: Tool for the unification of biology. Nat. Genet. 2000, 25, 25–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tatusov, R.L.; Galperin, M.Y.; Natale, D.A.; Koonin, E.V. The COG database: A tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 2000, 28, 33–36. [Google Scholar] [CrossRef] [Green Version]
- Consortium, U.P. UniProt: The universal protein knowledgebase in 2021. Nucleic Acids Res. 2020, 49, D480–D489. [Google Scholar] [CrossRef]
- Lyu, Y.Z.; Dong, X.Y.; Huang, L.B.; Zheng, J.W.; Jiang, Z.P. SLAF-seq Uncovers the Genetic Diversity and Adaptation of Chinese Elm (Ulmus parvifolia) in Eastern China. Forests 2020, 11, 80. [Google Scholar] [CrossRef] [Green Version]
- Fang, H.; Liu, H.; Ma, R.; Liu, Y.; Li, J.; Yu, X.; Zhang, H.; Yang, Y.; Zhang, G. Genome-wide assessment of population structure and genetic diversity of Chinese Lou onion using specific length amplified fragment (SLAF) sequencing. PLoS ONE 2020, 15, e0231753. [Google Scholar] [CrossRef] [PubMed]
- Zeng, B.; Yan, H.; Liu, X.; Zang, W.; Zhang, A.; Zhou, S.; Huang, L.; Liu, J. Genome-wide association study of rust traits in orchardgrass using SLAF-seq technology. Hereditas 2017, 154, 5. [Google Scholar] [CrossRef] [Green Version]
- Yang, J.; Zhang, C.; Zhao, N.; Zhang, L.; Hu, Z.; Chen, S.; Zhang, M. Chinese Root-type Mustard Provides Phylogenomic Insights into the Evolution of the Multi-use Diversified Allopolyploid Brassica juncea. Mol. Plant 2018, 11, 512–514. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, Y.; Tan, F.; Su, G.; Deng, S.; He, H.; Shi, S. Population genetic structure of three tree species in the mangrove genus Ceriops (Rhizophoraceae) from the Indo West Pacific. Genetica 2008, 133, 47–56. [Google Scholar] [CrossRef]
- Arnaud-Haond, S.; Teixeira, S.; Massa, S.I.; Billot, C.; Serråo, E.A. Genetic structure at range edge: Low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations. Mol. Ecol. 2010, 15, 3515–3525. [Google Scholar] [CrossRef] [PubMed]
- Tomimatsu, H.; Yamagishi, H.; Tanaka, I.; Sato, M.; Kondo, R.; Konno, Y. Consequences of forest fragmentation in an understory plant community: Extensive range expansion of native dwarf bamboo. Plant Species Biol. 2011, 26, 3–12. [Google Scholar] [CrossRef]
- Scholtz, R.; Polo, J.A.; Tanner, E.P.; Fuhlendorf, S.D. Grassland fragmentation and its influence on woody plant cover in the southern Great Plains, USA. Landsc. Ecol. 2018, 33, 1785–1797. [Google Scholar] [CrossRef]
- Kim, C.; Paterson, I.D.; Carla, L.; Hill, M.P. Expansive reed populations—Alien invasion or disturbed wetlands? Aob Plants 2018, 10, ply014. [Google Scholar]
- Hao, B.; Wu, H.; Shi, Q.; Liu, G.; Xing, W. Facilitation and competition among foundation species of submerged macrophytes threatened by severe eutrophication and implications for restoration. Ecol. Eng. 2013, 60, 76–80. [Google Scholar] [CrossRef]
- Valéry, L.; Radureau, A.; Lefeuvre, J.C. Spread of the native grass Elymus athericus in salt marshes of Mont-Saint-Michel bay as an unusual case of coastal eutrophication. J. Coast. Conserv. 2016, 21, 1–13. [Google Scholar] [CrossRef]
- Hangelbroek, H.H.; Ouborg, N.J.; Santamaría, L.; Schwenk, K. Clonal diversity and structure within a population of the pondweed Potamogeton pectinatus foraged by Bewick’s swans. Mol. Ecol. 2002, 11, 2137–2150. [Google Scholar] [CrossRef]
- Bona, A.; Kulesza, U.; Jadwiszczak, K.A. Clonal diversity, gene flow and seed production in endangered populations of Betula humilis Schrk. Tree Genet. Genomes 2019, 15, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Mikael, H.; Richard, L. Seed dispersal and fine-scale genetic structuring in the asexual Nigritella miniata (Orchidaceae) in the Alps. Bot. J. Linn. Soc. 2019, 190, 83–100. [Google Scholar]
- Brzosko, E.; Wróblewska, A.; Ratkiewicz, M. Spatial genetic structure and clonal diversity of island populations of lady’s slipper (Cypripedium calceolus) from the Biebrza National Park (Northeast Poland). Mol. Ecol. 2002, 11, 2499–2509. [Google Scholar] [CrossRef] [PubMed]
- Torimaru, T.; Tomaru, N.; Nishimura, N.; Yamamoto, S. Clonal diversity and genetic differentiation in Ilex leucoclada M. patches in an old-growth beech forest. Mol. Ecol. 2010, 12, 809–818. [Google Scholar] [CrossRef]
- Jacquemyn, H.; Brys, R.; Honnay, O.; Hermy, M.; Ruiz, I.R. Local forest environment largely affects below-ground growth, clonal diversity and fine-scale spatial genetic structure in the temperate deciduous forest herb Paris quadrifolia. Mol. Ecol. 2005, 14, 4479–4488. [Google Scholar] [CrossRef]
- Tang, S.Q.; Yuan, L.; Geng, Y.P.; Zhang, G.R.; Li, W.; Yang, Z. Clonal and spatial genetic structure in natural populations of Luohanguo (Siraitia grosvenorii), an economic species endemic to South China, as revealed by RAPD markers. Biochem. Syst. Ecol. 2007, 35, 557–565. [Google Scholar] [CrossRef]
- Peng, Y.L.; Macek, P.; Macková, J.; Romoleroux, K.; Hensen, I. Clonal Diversity and Fine-scale Genetic Structure in a High Andean Treeline Population. Biotropica 2015, 47, 59–65. [Google Scholar] [CrossRef]
- Leger, E.A.; Espeland, E.K.; Merrill, K.R.; Meyer, S.E. Genetic variation and local adaptation at a cheatgrass (Bromus tectorum) invasion edge in western Nevada. Mol. Ecol. 2009, 18, 4366–4379. [Google Scholar] [CrossRef] [PubMed]
- Kawecki, T.J.; Ebert, D. Conceptual issues in local adaptation. Ecol. Lett. 2004, 7, 1225–1241. [Google Scholar] [CrossRef] [Green Version]
- Wang, G.; Long, Y.; Thomma, B.; Wit, P.D.; Angenent, G.C.; Fiers, M. Functional Analyses of the CLAVATA2-Like Proteins and Their Domains That Contribute to CLAVATA2 Specificity. Plant Physiol. 2010, 152, 320–331. [Google Scholar] [CrossRef] [PubMed]
- Ohe, M.; Scoccianti, V.; Bagni, N.; Tassoni, A.; Matsuzaki, S. Putative occurrence of lysine decarboxylase isoforms in soybean (Glycine max) seedlings. Amino Acids 2009, 36, 65–70. [Google Scholar] [CrossRef] [PubMed]
Sites | GC Content (%) | Q30 (%) | Total SNPs | Number of SNPs | Hetloci Ratio of SNP (%) | Integrity Ratio of SNP (%) | Number of SLAFs | Average Sequencing Depth |
---|---|---|---|---|---|---|---|---|
Nansha | 38.94 | 93.37 | 360,672 | 91,102 | 8.29 | 25.25 | 215,124 | 15.22 |
Yangjiang | 39.87 | 91.93 | 360,672 | 91,277 | 10.83 | 25.30 | 207,818 | 13.99 |
Zhanjiang | 39.59 | 94.71 | 360,672 | 88,490 | 11.07 | 24.53 | 205,899 | 10.98 |
Sites | Average MAF | Ae | He | H | NPL | Ao | Ho | PIC | I |
---|---|---|---|---|---|---|---|---|---|
Nansha | 0.297 | 1.669 | 0.379 | 0.400 | 15,974 | 2 | 0.339 | 0.299 | 0.558 |
Yangjiang | 0.305 | 1.689 | 0.388 | 0.393 | 20,790 | 2 | 0.333 | 0.306 | 0.569 |
Zhanjiang | 0.308 | 1.696 | 0.391 | 0.396 | 17,698 | 2 | 0.277 | 0.307 | 0.572 |
Species level | 0.281 | 1.637 | 0.366 | 0.368 | 32,780 | 2 | 0.207 | 0.209 | 0.543 |
Population | G | N | NC | PD | D | E |
---|---|---|---|---|---|---|
Nansha | 7 | 12 | 1.71 | 0.58 | 0.91 | 0.84 |
Yangjiang | 30 | 54 | 1.80 | 0.56 | 0.97 | 0.93 |
Zhanjiang | 38 | 54 | 1.42 | 0.70 | 0.98 | 0.85 |
Environmental Factors | Marker ID | Annotation |
---|---|---|
Altitude | Marker39224 | PREDICTED: uncharacterized protein LOC102619730 |
Marker243205 | Receptor-like protein 12 | |
Mean daily temperature | Marker57755 | Integrase, catalytic region; zinc finger, CCHC-type; peptidase aspartic, catalytic |
Mean night temperature | Marker123428 | Hypothetical protein glysoja_029625 |
Marker102857 | Endonuclease/exonuclease/phosphatase family protein | |
NH4-N | Marker89512 | Possible lysine decarboxylase |
Marker24270 | Molecular Function: nucleic acid binding (GO:0003676); | |
Molecular Function: zinc ion binding (GO:0008270); | ||
Biological Process: DNA integration (GO:0015074) | ||
NH3-N | Marker184352 | Molecular Function: binding (GO:0005488) |
Marker302153 | PREDICTED: uncharacterized protein LOC105173347 | |
Marker123894 | Molecular Function: nucleic acid binding (GO:0003676); | |
Molecular Function: catalytic activity (GO:0003824); | ||
Biological Process: DNA metabolic process (GO:0006259) | ||
Marker301816 | Hypothetical protein MTR_3g040280 | |
Marker70724 | Hypothetical protein MTR_3g034520 | |
Marker42421 | Cellular Component: nucleus (GO:0005634); | |
Molecular Function: nucleotidyltransferase activity (GO:0016779); | ||
Biological Process: RNA 3’ uridylation (GO:0071076) | ||
Marker111233 | Molecular Function: nucleotide binding (GO:0000166); | |
Molecular Function: protein kinase activity (GO:0004672); | ||
Biological Process: phosphorylation (GO:0016310); | ||
K04733 interleukin-1 receptor-associated kinase 4 [EC:2.7.11.1] | ||
Organic matter | Marker183381 | PREDICTED: uncharacterized protein LOC105162605 |
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Zhang, Y.; Xin, K.; Liao, B.; Ai, X.; Sheng, N. The Genetic and Environmental Adaptation of the Associated Liana Species Derris trifoliata Lour. (Leguminosae) in Mangroves. Forests 2021, 12, 1375. https://doi.org/10.3390/f12101375
Zhang Y, Xin K, Liao B, Ai X, Sheng N. The Genetic and Environmental Adaptation of the Associated Liana Species Derris trifoliata Lour. (Leguminosae) in Mangroves. Forests. 2021; 12(10):1375. https://doi.org/10.3390/f12101375
Chicago/Turabian StyleZhang, Yun, Kun Xin, Baowen Liao, Xihang Ai, and Nong Sheng. 2021. "The Genetic and Environmental Adaptation of the Associated Liana Species Derris trifoliata Lour. (Leguminosae) in Mangroves" Forests 12, no. 10: 1375. https://doi.org/10.3390/f12101375
APA StyleZhang, Y., Xin, K., Liao, B., Ai, X., & Sheng, N. (2021). The Genetic and Environmental Adaptation of the Associated Liana Species Derris trifoliata Lour. (Leguminosae) in Mangroves. Forests, 12(10), 1375. https://doi.org/10.3390/f12101375