A Single Hemoglobin Gene in Myrica Gale Retains Both Symbiotic and Non-symbiotic Specificity

Overview

Journal Plant Mol Biol

Date 2006 Aug 10

PMID 16897491

Citations 12

Authors

Anne B Heckmann

Kim H Hebelstrup

Knud Larsen

Nuno M Micaelo

Erik O Jensen

Affiliations

Soon will be listed here.

Abstract

Here, a hemoglobin gene from the nitrogen-fixing actinorhizal plant Myrica gale was isolated, cloned and sequenced. The gene (MgHb) was a class I hemoglobin with strong sequence homology to non-symbiotic hemoglobin genes. MgHb is highly expressed in symbiotic root nodules, but transcripts and protein were also detected in leaves of M. gale. In Arabidopsis thaliana the MgHb promoter, linked to a beta-glucuronidase coding region, directed expression in the vascular tissue, in shoot meristem and at root branch point--a pattern very similar to the combined expression pattern of the two non-symbiotic A. thaliana hemoglobin promoters AHb1 and AHb2. The results points to a symbiotic as well as a non-symbiotic specificity of MgHb similar to a hemoglobin gene identified in Parasponia andersonii, but different from the situation in Casuarina glauca--a close actinorhizal relative of M. gale.

Citing Articles

A Roadmap toward Engineered Nitrogen-Fixing Nodule Symbiosis.

Huisman R, Geurts R Plant Commun. 2021; 1(1):100019.

PMID: 33404552 PMC: 7748023. DOI: 10.1016/j.xplc.2019.100019.

The Evolutionary Aspects of Legume Nitrogen-Fixing Nodule Symbiosis.

Shen D, Bisseling T Results Probl Cell Differ. 2020; 69:387-408.

PMID: 33263880 DOI: 10.1007/978-3-030-51849-3_14.

Nitric oxide function during oxygen deprivation in physiological and stress processes.

Manrique-Gil I, Sanchez-Vicente I, Torres-Quezada I, Lorenzo O J Exp Bot. 2020; 72(3):904-916.

PMID: 32976588 PMC: 7876777. DOI: 10.1093/jxb/eraa442.

Comparative Analysis of the Nodule Transcriptomes of (Rhamnaceae, Rosales) and (Datiscaceae, Cucurbitales).

Salgado M, van Velzen R, Van Nguyen T, Battenberg K, Berry A, Lundin D Front Plant Sci. 2018; 9:1629.

PMID: 30487804 PMC: 6246699. DOI: 10.3389/fpls.2018.01629.

Genetic diversity of male and female Chinese bayberry (Myrica rubra) populations and identification of sex-associated markers.

Jia H, Jiao Y, Wang G, Li Y, Jia H, Wu H BMC Genomics. 2015; 16:394.

PMID: 25986380 PMC: 4436740. DOI: 10.1186/s12864-015-1602-5.

References

Taylor E, Nie X, Macgregor A, Hill R . A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Mol Biol. 1994; 24(6):853-62. DOI: 10.1007/BF00014440. View

Dilworth M . The plant as the genetic determinant of leghaemoglobin production in the legume root nodule. Biochim Biophys Acta. 1969; 184(2):432-41. DOI: 10.1016/0304-4165(69)90047-6. View

Bogusz D, Llewellyn D, Craig S, Dennis E, Appleby C, Peacock W . Nonlegume hemoglobin genes retain organ-specific expression in heterologous transgenic plants. Plant Cell. 1990; 2(7):633-41. PMC: 159917. DOI: 10.1105/tpc.2.7.633. View

Vieweg M, Hohnjec N, Kuster H . Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. Planta. 2004; 220(5):757-66. DOI: 10.1007/s00425-004-1397-0. View

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

Appleby C, Tjepkema J, Trinick M . Hemoglobin in a nonleguminous plant, parasponia: possible genetic origin and function in nitrogen fixation. Science. 1983; 220(4600):951-3. DOI: 10.1126/science.220.4600.951. View

Hunt P, Watts R, Trevaskis B, Llewelyn D, Burnell J, Dennis E . Expression and evolution of functionally distinct haemoglobin genes in plants. Plant Mol Biol. 2001; 47(5):677-92. DOI: 10.1023/a:1012440926982. View

Anderson C, Jensen E, Llewellyn D, Dennis E, Peacock W . A new hemoglobin gene from soybean: a role for hemoglobin in all plants. Proc Natl Acad Sci U S A. 1996; 93(12):5682-7. PMC: 39120. DOI: 10.1073/pnas.93.12.5682. View

Ott T, van Dongen J, Gunther C, Krusell L, Desbrosses G, Vigeolas H . Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr Biol. 2005; 15(6):531-5. DOI: 10.1016/j.cub.2005.01.042. View

10.

Christensen T, Dennis E, Peacock J, Landsmann J, Marcker K . Hemoglobin genes in non-legumes: cloning and characterization of a Casuarina glauca hemoglobin gene. Plant Mol Biol. 1991; 16(2):339-44. DOI: 10.1007/BF00020566. View

11.

Sandal N, Bojsen K, Marcker K . A small family of nodule specific genes from soybean. Nucleic Acids Res. 1987; 15(4):1507-19. PMC: 340564. DOI: 10.1093/nar/15.4.1507. View

12.

Watts R, Hunt P, Hvitved A, Hargrove M, Peacock W, Dennis E . A hemoglobin from plants homologous to truncated hemoglobins of microorganisms. Proc Natl Acad Sci U S A. 2001; 98(18):10119-24. PMC: 56925. DOI: 10.1073/pnas.191349198. View

13.

Dordas C, Hasinoff B, Rivoal J, Hill R . Class-1 hemoglobins, nitrate and NO levels in anoxic maize cell-suspension cultures. Planta. 2004; 219(1):66-72. DOI: 10.1007/s00425-004-1212-y. View

14.

Igamberdiev A, Hill R . Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. J Exp Bot. 2004; 55(408):2473-82. DOI: 10.1093/jxb/erh272. View

15.

Uchiumi T, Shimoda Y, Tsuruta T, Mukoyoshi Y, Suzuki A, Senoo K . Expression of symbiotic and nonsymbiotic globin genes responding to microsymbionts on Lotus japonicus. Plant Cell Physiol. 2002; 43(11):1351-8. DOI: 10.1093/pcp/pcf165. View

16.

Duff S, Wittenberg J, Hill R . Expression, purification, and properties of recombinant barley (Hordeum sp.) hemoglobin. Optical spectra and reactions with gaseous ligands. J Biol Chem. 1997; 272(27):16746-52. DOI: 10.1074/jbc.272.27.16746. View

17.

Bogusz D, Appleby C, Landsmann J, Dennis E, Trinick M, Peacock W . Functioning haemoglobin genes in non-nodulating plants. Nature. 1988; 331(6152):178-80. DOI: 10.1038/331178a0. View

18.

Trevaskis B, Watts R, Andersson C, Llewellyn D, Hargrove M, Olson J . Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. Proc Natl Acad Sci U S A. 1997; 94(22):12230-4. PMC: 23758. DOI: 10.1073/pnas.94.22.12230. View

19.

Pathirana S, Tjepkema J . Purification of Hemoglobin from the Actinorhizal Root Nodules of Myrica gale L. Plant Physiol. 1995; 107(3):827-831. PMC: 157199. DOI: 10.1104/pp.107.3.827. View

20.

Tjepkema J, Cashon R, Beckwith J, Schwintzer C . Hemoglobin in Frankia, a nitrogen-fixing actinomycete. Appl Environ Microbiol. 2002; 68(5):2629-31. PMC: 127563. DOI: 10.1128/AEM.68.5.2629-2631.2002. View