Rhizophora spp.


Rhizophora spp. in Papua New Guinea. In the absence of hurricanes and chain saws, individual trees may reach 40m or more. Photo courtesy of Barry Clough.

The genus Rhizophora contains more species of mangrove than any other. Their tangled prop root systems – illustrated in the header photo – are the “trademark” associated with all mangroves by most people (if they have heard of them at all). In the equatorial zones of New Guinea and Darien Province (Panama) individual trees may reach heights of 40 m.  More generally, they are much shorter, and on some off-shore, eXtremely oligotrophic, peat-based islands, 50+ year old trees may be no more than a meter tall.

The genus is thought to have originally evolved at the eastern, Indo-Pacific, end of the Tethys Sea. American, west African and eastern Pacific species evolved following dispersal westward before the Mediterranean closed off.1  The Rhizophora fossil record begins with pollen in Australia 60 MYA; by 40 MYA, fossil evidence shows expansion to North America, Panama, south-west Australia, India and Borneo. See the Mangroves page for more discussion of evolution.

Today, there are 6 recognized Rhizophora species and 4 hybrids. Transcriptomic or genomic resources are available for R. mangle 2, R. apiculata (in press), R. mucronata (no publications) and R. stylosa (240 ESTs). Unfortunately, none of these has been extended to comparative transcriptomics and the network analyses that can give the most state-of-the-art indications of the links between the genome and organismal behavior. These will require in depth analysis of different treatments or conditions and will undoubtedly – or at least, hopefully – be available in due time.

Applying genomics

Can genomic/transcriptomic tools be used to answer physiological and ecological questions?

Once comparative transcriptomic and network analysis tools have been developed, the number of addressable questions will approach the infinite.  Some are immediately of practical interest.  For example, how different are the organizations and details genomes of the Rhizophora species? Are they sufficiently similar that the genome of, say, R. apiculata can be used to study transcriptome expression patterns in R. stylosa? So far, the answer looks like it might be “yes”. Has the water-borne propagule dispersal mechanism resulted in sufficiently low variability in gene sequences that multiple individual samples can be pooled in transcriptome studies?

Cross section of a mature R. mangle leaf stained with haemotoxylon and eosin to reveal tannins (yellow, “t”) and flavologlycans (“slime” – purple, “f”). The palisades cells, below the “slime cells” are small (“p”).3

But perhaps the most interesting questions about Rhizophora mangroves (a class highly susceptible to personal opinion), may be approachable using molecular tools. Basically, it comes down to the same questions asked by plant biologists forever – “how do they do it?”  For example, how do propagules control their buoyancy or assure that they germinate only after establishing physical contact with a substrate? 4  Or, what are the fundamental changes associated with the response of stunted (“dwarf”) mangroves to phosphorous?567 Or, how do individuals cope with tides that range by 2 m or more daily, with even larger seasonal ranges, some of which leave them high and dry? Or, how and to what effect do the leaves accumulate more than 50% of their dry mass in polyphenolics, condensed tannins and flavologlycans? 8

Genome resources

Recent advances at the molecular level

As noted on the general mangrove page, much or most of the recent work on Rhizophora has originated in the lab of Suhua Shi (Sun Yat-Sen University, Guangzhou, China). They have particularly addressed a number of aspects of Rhizophora evolution showing that the genus is particularly appropriate for exploring biogeography, molecular evolution, population genetics, hybridization and conservation genetics. Chen et al. 9, for example, developed a suite of nuclear gene primers which showed applicability across five Rhizophora species. They applied those to populations in the Hainan (China) area for (a) reconstruction of Rhizophoracean phylogeny, (b) examination of the structure of Rhizophora genomes, and (c) identification of natural hybridization in the genus.

The first application supported the hypothesis that the established migration of Rhizophora to the proto-Atlantic was, in fact, unsuccessful, and that the region was re-colonized from the IWP region approximately 12.7 MYA in spite of the closure of the Mediterranean at 18 MYA. Examination of the genome structures in four natural populations of R. apiculata (topic b) revealed extremely low genetic diversity but a strong influence of recent glaciations on the population dynamics of R. apiculata. Finally, they were able to verify that a morphologically intermediate individual between R. apiculata and R. stylosa was, in fact, a hybrid.

In a more recent paper from the same lab, Xu, He et al.10 considered convergence at the gene level that might be expected in association with phenotypic convergence to the mangrove habitat.  That study has been highlighted elsewhere on this site.

Most recently, the Shi group has compared the transcriptomes of four rhizophoracean species (Bruguiera gymnorhiza, Kandelia obovata, Rhizophora apiculata, and Ceriops tagal), and Carallia brachiata, a terrestrial member of the family. 11 The transcriptome profiles were similar among the five species – a potentially very useful finding in itself – but genomic characteristics conserved across the four mangrove species differed from those of Ca. brachiata.  Using an approach similar to that they employed with the mangrove fern, Acrostichum aureum12, they used these resources to consider the origin and evolution of the Rhizophoraceae, identifying 10 positively selected genes from the ancestor branch of the family, mainly associated with GO biological processes of stress response (a very broad and potentially meaningless class), embryo development, and regulation of gene expression (also perhaps too broad a classification to really be useful). Positive selection of these genes may have been crucial to the adaptation of the trees to stressful intertidal environments.

Literature resources

Resources from the literature

The following list was generated by searching PubMed, limiting the list to 100 references.  As there are many journals not indexed there, this list will be incomplete.

  1. Short, AW, Sebastian, JSV, Huang, J, Wang, G, Dassanayake, M, Finnegan, PM et al. (2024) Comparative transcriptomics of the chilling stress response in two Asian mangrove species, Bruguiera gymnorhiza and Rhizophora apiculata. Tree Physiol 44:. doi: 10.1093/treephys/tpae019. PubMed PMID:38366388 .
  2. Zhang, Y, Yang, Y, He, M, Wei, Z, Qin, X, Wu, Y et al. (2023) Comparative chloroplast genome analyses provide insights into evolutionary history of Rhizophoraceae mangroves. PeerJ 11:e16400. doi: 10.7717/peerj.16400. PubMed PMID:38025714 PubMed Central PMC10658886.
  3. Chang, LF, Fei, J, Wang, YS, Ma, XY, Zhao, Y, Cheng, H et al. (2023) Comparative Analysis of Cd Uptake and Tolerance in Two Mangrove Species (Avicennia marina and Rhizophora stylosa) with Distinct Apoplast Barriers. Plants (Basel) 12:. doi: 10.3390/plants12223786. PubMed PMID:38005683 PubMed Central PMC10674663.
  4. Shijili, M, Valsalan, R, Mathew, D (2023) Genome wide identification and characterization of MATE family genes in mangrove plants. Genetica 151:241-249. doi: 10.1007/s10709-023-00186-w. PubMed PMID:37014491 .
  5. Piro, A, Mazzuca, S, Phandee, S, Jenke, M, Buapet, P (2023) Physiology and proteomics analyses reveal the response mechanisms of Rhizophora mucronata seedlings to prolonged complete submergence. Plant Biol (Stuttg) 25:420-432. doi: 10.1111/plb.13503. PubMed PMID:36689309 .
  6. Pootakham, W, Naktang, C, Sonthirod, C, Kongkachana, W, Narong, N, Sangsrakru, D et al. (2022) Chromosome-level genome assembly of Indian mangrove (Ceriops tagal) revealed a genome-wide duplication event predating the divergence of Rhizophoraceae mangrove species. Plant Genome 15:e20217. doi: 10.1002/tpg2.20217. PubMed PMID:35608212 .
  7. Xu, S, Guo, Z, Feng, X, Shao, S, Yang, Y, Li, J et al. (2023) Where whole-genome duplication is most beneficial: Adaptation of mangroves to a wide salinity range between land and sea. Mol Ecol 32:460-475. doi: 10.1111/mec.16320. PubMed PMID:34882881 .
  8. Miryeganeh, M, Saze, H (2021) The First De Novo Transcriptome Assembly and Transcriptomic Dynamics of the Mangrove Tree Rhizophora stylosa Griff. (Rhizophoraceae). Int J Mol Sci 22:. doi: 10.3390/ijms222111964. PubMed PMID:34769393 PubMed Central PMC8584393.
  9. Wang, Y, Huang, C, Zeng, W, Zhang, T, Zhong, C, Deng, S et al. (2021) Epigenetic and transcriptional responses underlying mangrove adaptation to UV-B. iScience 24:103148. doi: 10.1016/j.isci.2021.103148. PubMed PMID:34646986 PubMed Central PMC8496181.
  10. Mounger, J, Boquete, MT, Schmid, MW, Granado, R, Robertson, MH, Voors, SA et al. (2021) Inheritance of DNA methylation differences in the mangrove Rhizophora mangle. Evol Dev 23:351-374. doi: 10.1111/ede.12388. PubMed PMID:34382741 .
  11. Azman, A, Ng, KK, Ng, CH, Lee, CT, Tnah, LH, Zakaria, NF et al. (2020) Low genetic diversity indicating the threatened status of Rhizophora apiculata (Rhizophoraceae) in Malaysia: declined evolution meets habitat destruction. Sci Rep 10:19112. doi: 10.1038/s41598-020-76092-4. PubMed PMID:33154411 PubMed Central PMC7644706.
  12. Han, K, Shi, C, Li, L, Seim, I, Lee, SM, Xu, X et al. (2020) Lineage-specific evolution of mangrove plastid genomes. Plant Genome 13:e20019. doi: 10.1002/tpg2.20019. PubMed PMID:33016609 .
  13. Meera, SP, Augustine, A (2020) De novo transcriptome analysis of Rhizophora mucronata Lam. furnishes evidence for the existence of glyoxalase system correlated to glutathione metabolic enzymes and glutathione regulated transporter in salt tolerant mangroves. Plant Physiol Biochem 155:683-696. doi: 10.1016/j.plaphy.2020.08.008. PubMed PMID:32861035 .
  14. Nualla-Ong, A, Phongdara, A, Buapet, P (2020) Copper and zinc differentially affect root glutathione accumulation and phytochelatin synthase gene expression of Rhizophora mucronata seedlings: Implications for mechanisms underlying trace metal tolerance. Ecotoxicol Environ Saf 205:111175. doi: 10.1016/j.ecoenv.2020.111175. PubMed PMID:32836161 .
  15. Shi, C, Han, K, Li, L, Seim, I, Lee, SM, Xu, X et al. (2020) Complete Chloroplast Genomes of 14 Mangroves: Phylogenetic and Comparative Genomic Analyses. Biomed Res Int 2020:8731857. doi: 10.1155/2020/8731857. PubMed PMID:32462024 PubMed Central PMC7225854.
  16. Torasa, S, Boonyarat, P, Phongdara, A, Buapet, P (2019) Tolerance Mechanisms to Copper and Zinc Excess in Rhizophora mucronata Lam. Seedlings Involve Cell Wall Sequestration and Limited Translocation. Bull Environ Contam Toxicol 102:573-580. doi: 10.1007/s00128-019-02589-y. PubMed PMID:30868179 .
  17. Hodel, RGJ, Knowles, LL, McDaniel, SF, Payton, AC, Dunaway, JF, Soltis, PS et al. (2018) Terrestrial species adapted to sea dispersal: Differences in propagule dispersal of two Caribbean mangroves. Mol Ecol 27:4612-4626. doi: 10.1111/mec.14894. PubMed PMID:30308703 .
  18. Bajay, SK, Cruz, MV, da Silva, CC, Murad, NF, Brandão, MM, de Souza, AP et al. (2018) Extremophiles as a Model of a Natural Ecosystem: Transcriptional Coordination of Genes Reveals Distinct Selective Responses of Plants Under Climate Change Scenarios. Front Plant Sci 9:1376. doi: 10.3389/fpls.2018.01376. PubMed PMID:30283484 PubMed Central PMC6156123.
  19. Wang, Y, Liang, W, Tang, T (2018) Constant conflict between Gypsy LTR retrotransposons and CHH methylation within a stress-adapted mangrove genome. New Phytol 220:922-935. doi: 10.1111/nph.15209. PubMed PMID:29762876 .
  20. Hodel, RGJ, Chen, S, Payton, AC, McDaniel, SF, Soltis, P, Soltis, DE et al. (2017) Adding loci improves phylogeographic resolution in red mangroves despite increased missing data: comparing microsatellites and RAD-Seq and investigating loci filtering. Sci Rep 7:17598. doi: 10.1038/s41598-017-16810-7. PubMed PMID:29242627 PubMed Central PMC5730610.
  21. Xu, S, He, Z, Zhang, Z, Guo, Z, Guo, W, Lyu, H et al. (2017) The origin, diversification and adaptation of a major mangrove clade (Rhizophoreae) revealed by whole-genome sequencing. Natl Sci Rev 4:721-734. doi: 10.1093/nsr/nwx065. PubMed PMID:31258950 PubMed Central PMC6599620.
  22. Kennedy, JP, Pil, MW, Proffitt, CE, Boeger, WA, Stanford, AM, Devlin, DJ et al. (2016) Postglacial expansion pathways of red mangrove, Rhizophora mangle, in the Caribbean Basin and Florida. Am J Bot 103:260-76. doi: 10.3732/ajb.1500183. PubMed PMID:26838364 .
  23. Gharat, SA, Shaw, BP (2015) Novel and conserved miRNAs in the halophyte Suaeda maritima identified by deep sequencing and computational predictions using the ESTs of two mangrove plants. BMC Plant Biol 15:301. doi: 10.1186/s12870-015-0682-3. PubMed PMID:26714456 PubMed Central PMC4696257.
  24. Chen, Y, Hou, Y, Guo, Z, Wang, W, Zhong, C, Zhou, R et al. (2015) Applications of Multiple Nuclear Genes to the Molecular Phylogeny, Population Genetics and Hybrid Identification in the Mangrove Genus Rhizophora. PLoS One 10:e0145058. doi: 10.1371/journal.pone.0145058. PubMed PMID:26674070 PubMed Central PMC4682636.
  25. Wee, AK, Takayama, K, Chua, JL, Asakawa, T, Meenakshisundaram, SH, Onrizal, et al. (2015) Genetic differentiation and phylogeography of partially sympatric species complex Rhizophora mucronata Lam. and R. stylosa Griff. using SSR markers. BMC Evol Biol 15:57. doi: 10.1186/s12862-015-0331-3. PubMed PMID:25888261 PubMed Central PMC4389924.
  26. Lo, EY, Duke, NC, Sun, M (2014) Phylogeographic pattern of Rhizophora (Rhizophoraceae) reveals the importance of both vicariance and long-distance oceanic dispersal to modern mangrove distribution. BMC Evol Biol 14:83. doi: 10.1186/1471-2148-14-83. PubMed PMID:24742016 PubMed Central PMC4021169.
  27. Sandoval-Castro, E, Dodd, RS, Riosmena-Rodríguez, R, Enríquez-Paredes, LM, Tovilla-Hernández, C, López-Vivas, JM et al. (2014) Post-glacial expansion and population genetic divergence of mangrove species Avicennia germinans (L.) Stearn and Rhizophora mangle L. along the Mexican coast. PLoS One 9:e93358. doi: 10.1371/journal.pone.0093358. PubMed PMID:24699389 PubMed Central PMC3974753.
  28. Sahebi, M, Hanafi, MM, Abdullah, SN, Rafii, MY, Azizi, P, Nejat, N et al. (2014) Isolation and expression analysis of novel silicon absorption gene from roots of mangrove (Rhizophora apiculata) via suppression subtractive hybridization. Biomed Res Int 2014:971985. doi: 10.1155/2014/971985. PubMed PMID:24516858 PubMed Central PMC3910099.
  29. Gurudeeban, S, Satyavani, K, Ramanathan, T (2013) Phylogeny of Indian rhizophoraceae based on the molecular data from chloroplast tRNA(LEU)UAA intergenic sequences. Pak J Biol Sci 16:1130-7. doi: 10.3923/pjbs.2013.1130.1137. PubMed PMID:24506012 .
  30. Yahya, AF, Hyun, JO, Lee, JH, Kim, YY, Lee, KM, Hong, KN et al. (2014) Genetic variation and population genetic structure of Rhizophora apiculata (Rhizophoraceae) in the Greater Sunda Islands, Indonesia using microsatellite markers. J Plant Res 127:287-97. doi: 10.1007/s10265-013-0613-z. PubMed PMID:24323307 .
  31. Takayama, K, Tamura, M, Tateishi, Y, Webb, EL, Kajita, T (2013) Strong genetic structure over the American continents and transoceanic dispersal in the mangrove genus Rhizophora (Rhizophoraceae) revealed by broad-scale nuclear and chloroplast DNA analysis. Am J Bot 100:1191-201. doi: 10.3732/ajb.1200567. PubMed PMID:23711904 .
  32. Cerón-Souza, I, Bermingham, E, McMillan, WO, Jones, FA (2012) Comparative genetic structure of two mangrove species in Caribbean and Pacific estuaries of Panama. BMC Evol Biol 12:205. doi: 10.1186/1471-2148-12-205. PubMed PMID:23078287 PubMed Central PMC3543234.
  33. Pil, MW, Boeger, MR, Muschner, VC, Pie, MR, Ostrensky, A, Boeger, WA et al. (2011) Postglacial north-south expansion of populations of Rhizophora mangle (Rhizophoraceae) along the Brazilian coast revealed by microsatellite analysis. Am J Bot 98:1031-9. doi: 10.3732/ajb.1000392. PubMed PMID:21653512 .
  34. Dassanayake, M, Haas, JS, Bohnert, HJ, Cheeseman, JM (2009) Shedding light on an extremophile lifestyle through transcriptomics. New Phytol 183:764-775. doi: 10.1111/j.1469-8137.2009.02913.x. PubMed PMID:19549131 .
  35. Huang, W, Fang, XD, Lin, QF, Li, GY, Zhao, WM (2003) Identification and expression analysis of a full-length cDNA encoding a Kandelia candel tonoplast intrinsic protein. Sheng Wu Gong Cheng Xue Bao 19:147-52. . PubMed PMID:15966312 .
  36. Mukherjee, AK, Acharya, L, Panda, PC, Mohapatra, T, Das, P (2004) Genomic relations among two non-mangrove and nine mangrove species of Indian Rhizophoraceae. Z Naturforsch C J Biosci 59:572-8. doi: 10.1515/znc-2004-7-822. PubMed PMID:15813382 .
  37. Parani, M, Rajesh, K, Lakshmi, M, Parducci, L, Szmidt, AE, Parida, A et al. (2001) Species identification in seven small millet species using polymerase chain reaction-restriction fragment length polymorphism of trnS-psbC gene region. Genome 44:495-9. doi: 10.1139/g01-023. PubMed PMID:11444709 .
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