The ubiquity and coexistence of two FBPases in chloroplasts of photosynthetic eukaryotes and its evolutionary and functional implications

doi:10.1016/j.pld.2019.09.002

Plant Diversity ›› 2020, Vol. 42 ›› Issue (02): 120-125.DOI: 10.1016/j.pld.2019.09.002

• Articles • 上一篇

The ubiquity and coexistence of two FBPases in chloroplasts of photosynthetic eukaryotes and its evolutionary and functional implications

Yujin Li^a,b, Qingqing Ye^a, De He^c, Huixian Bai^a, Jianfan Wen^a

a State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, 650223, China;
b Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan, 650204, China;
c College of Life Sciences, Southwest Forestry University, Kunming, Yunnan, 650224, China

收稿日期:2019-05-23 修回日期:2019-08-27 出版日期:2020-04-25 发布日期:2020-04-30
通讯作者: Jianfan Wen
基金资助:
This research was funded by the National Natural Science Foundation of China (31572256 and 31801967) and State Key Laboratory of Genetic Resources and Evolution (GREKF17-03).

The ubiquity and coexistence of two FBPases in chloroplasts of photosynthetic eukaryotes and its evolutionary and functional implications

Yujin Li^a,b, Qingqing Ye^a, De He^c, Huixian Bai^a, Jianfan Wen^a

a State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, 650223, China;
b Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan, 650204, China;
c College of Life Sciences, Southwest Forestry University, Kunming, Yunnan, 650224, China

Received:2019-05-23 Revised:2019-08-27 Online:2020-04-25 Published:2020-04-30
Supported by:
This research was funded by the National Natural Science Foundation of China (31572256 and 31801967) and State Key Laboratory of Genetic Resources and Evolution (GREKF17-03).

摘要/Abstract

摘要： In photosynthetic eukaryotes, there are two well-characterized fructose-1,6-bisphosphatases (FBPases): the redox-insensitive cytosolic FBPase (cyFBPase), which participates in gluconeogenesis, and the redoxsensitive chloroplastic FBPase (cpFBPase1), which is a critical enzyme in the Calvin cycle. Recent studies have identified a new chloroplastic FBPase, cpFBPase2; however, its phylogenetic distribution, evolutionary origin, and physiological function remain unclear. In this study, we identified and characterized these three FBPase isoforms in diverse, representative photosynthetic lineages and analyzed their phylogeny. In contrast to previous hypotheses, we found that cpFBPase2 is ubiquitous in photosynthetic eukaryotes. Additionally, all cpFBPase2s from diverse lineages form a monophyly, suggesting cpFBPase2 is not a recently evolved enzyme restricted to land plants but rather evolved early in the evolution of photosynthetic organisms, and most likely, in the common ancestor of photosynthetic eukaryotes. cyFBPase was probably first duplicated to produce cpFBPase2, and then the latter duplicated to produce cpFBPase1. The ubiquitous coexistence of these two cpFBPases in chloroplasts is most likely the consequence of adaptation to different redox conditions of photosynthesis, especially those caused by recurrent changes in light conditions.

关键词: FBPase, Photosynthetic eukaryotes, Coexistence, Evolution, Adaptation

Abstract: In photosynthetic eukaryotes, there are two well-characterized fructose-1,6-bisphosphatases (FBPases): the redox-insensitive cytosolic FBPase (cyFBPase), which participates in gluconeogenesis, and the redoxsensitive chloroplastic FBPase (cpFBPase1), which is a critical enzyme in the Calvin cycle. Recent studies have identified a new chloroplastic FBPase, cpFBPase2; however, its phylogenetic distribution, evolutionary origin, and physiological function remain unclear. In this study, we identified and characterized these three FBPase isoforms in diverse, representative photosynthetic lineages and analyzed their phylogeny. In contrast to previous hypotheses, we found that cpFBPase2 is ubiquitous in photosynthetic eukaryotes. Additionally, all cpFBPase2s from diverse lineages form a monophyly, suggesting cpFBPase2 is not a recently evolved enzyme restricted to land plants but rather evolved early in the evolution of photosynthetic organisms, and most likely, in the common ancestor of photosynthetic eukaryotes. cyFBPase was probably first duplicated to produce cpFBPase2, and then the latter duplicated to produce cpFBPase1. The ubiquitous coexistence of these two cpFBPases in chloroplasts is most likely the consequence of adaptation to different redox conditions of photosynthesis, especially those caused by recurrent changes in light conditions.

Key words: FBPase, Photosynthetic eukaryotes, Coexistence, Evolution, Adaptation

Yujin Li, Qingqing Ye, De He, Huixian Bai, Jianfan Wen. The ubiquity and coexistence of two FBPases in chloroplasts of photosynthetic eukaryotes and its evolutionary and functional implications[J]. Plant Diversity, 2020, 42(02): 120-125.

参考文献

Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., 1990. Basic local alignment search tool. J. Mol. Biol. 215, 403-410. https://doi.org/10.1016/s0022-2836(05)80360-2.
Armougom, F., Moretti, S., Poirot, O., Audic, S., Dumas, P., Schaeli, B., Keduas, V., Notredame, C., 2006. Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-coffee. Nucleic Acids Res. 34, W604-W608. https://doi.org/10.1093/nar/gkl092.
Blanc, G., Duncan, G., Agarkova, I., Borodovsky, M., Gurnon, J., Kuo, A., Lindquist, E., Lucas, S., Pangilinan, J., Polle, J., Salamov, A., Terry, A., Yamada, T., Dunigan, D.D., Grigoriev, I.V., Claverie, J.-M., Van Etten, J.L., 2010. The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22, 2943-2955. https://doi.org/10.1105/tpc.110.076406.
Bogen, C., Al-Dilaimi, A., Albersmeier, A., Wichmann, J., Grundmann, M., Rupp, O., Lauersen, K.J., Blifernez-Klassen, O., Kalinowski, J., Goesmann, A., Mussgnug, J.H., Kruse, O., 2013. Reconstruction of the lipid metabolism for the microalga Monoraphidium neglectum from its genome sequence reveals characteristics suitable for biofuel production. BMC Genomics 14. https://doi.org/10.1186/1471-2164-14-926.
Brawley, S.H., Blouin, N.A., Ficko-Blean, E., Wheeler, G.L., Lohr, M., Goodson, H.V., Jenkins, J.W., Blaby-Haas, C.E., Helliwell, K.E., Chan, C.X., Marriage, T.N., Bhattacharya, D., Klein, A.S., Badis, Y., Brodie, J., Cao, Y., Collen, J., Dittami, S.M., Gachon, C.M.M., Green, B.R., Karpowicz, S.J., Kim, J.W., Kudahl, U.J., Lin, S., Michel, G., Mittag, M., Olson, B.J.S.C., Pangilinan, J.L., Peng, Y., Qiu, H., Shu, S., Singer, J.T., Smith, A.G., Sprecher, B.N., Wagner, V., Wang, W., Wang, Z.-Y., Yan, J., Yarish, C., Zauner-Riek, S., Zhuang, Y., Zou, Y., Lindquist, E.A., Grimwood, J., Barry, K.W., Rokhsar, D.S., Schmutz, J., Stiller, J.W., Grossman, A.R., Prochnik, S.E., 2017. Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proc. Natl. Acad. Sci. U. S. A 114, E6361-E6370. https://doi.org/10.1073/pnas.1703088114.
Brown, G., Singer, A., Lunin, V.V., Proudfoot, M., Skarina, T., Flick, R., Kochinyan, S., Sanishvili, R., Joachimiak, A., Edwards, A.M., 2009. Structural and biochemical characterization of the type II fructose-1, 6-bisphosphatase GlpX from Escherichia coli. J. Biol. Chem. 284, 3784-3792. https://doi.org/10.1074/jbc.M808186200.
Buchanan, B.B., 1980. Role of light in the regulation of chloroplast enzymes. Annu.Rev. Plant Physiol. Plant Mol. Biol. 31, 341-374. https://doi.org/10.1146/annurev.pp.31.060180.002013.
Chiadmi, M., Navaza, A., Miginiac-Maslow, M., Jacquot, J.P., Cherfils, J., 1999. Redox signalling in the chloroplast: structure of oxidized pea fructose-1,6-bisphosphate phosphatase. EMBO J. 18, 6809-6815. https://doi.org/10.1093/emboj/18.23.6809.
Chueca, A., Sahrawy, M., Pagano, E.A., Gorge, J.L., 2002. Chloroplast fructose-1,6-bisphosphatase: structure and function. Photosynth. Res. 74, 235-249.https://doi.org/10.1023/a:1021243110495.
Collen, J., Porcel, B., Carre, W., Ball, S.G., Chaparro, C., Tonon, T., Barbeyron, T., Michel, G., Noel, B., Valentin, K., Elias, M., Artiguenave, F., Arun, A., Aury, J.-M., Barbosa-Neto, J.F., Bothwell, J.H., Bouget, F.-Y., Brillet, L., Cabello-Hurtado, F., Capella-Gutierrez, S., Charrier, B., Cladiere, L., Cock, J.M., Coelho, S.M., Colleoni, C., Czjzek, M., Da Silva, C., Delage, L., Denoeud, F., Deschamps, P., Dittami, S.M., Gabaldon, T., Gachon, C.M.M., Groisillier, A., Herve, C., Jabbari, K., Katinka, M., Kloareg, B., Kowalczyk, N., Labadie, K., Leblanc, C., Lopez, P.J., McLachlan, D.H., Meslet-Cladiere, L., Moustafa, A., Nehr, Z., Collen, P.N., Panaud, O., Partensky, F., Poulain, J., Rensing, S.A., Rousvoal, S., Samson, G., Symeonidi, A., Weissenbach, J., Zambounis, A., Wincker, P., Boyen, C., 2013.
Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc. Natl. Acad. Sci. U. S. A 110, 5247-5252. https://doi.org/10.1073/pnas.1221259110.
Cseke, C., Buchanan, B.B., 1986. Regulation of the formation and utilization of photosynthate in leaves. Biochim. Biophys. Acta 853, 43-63. https://doi.org/10.1016/0304-4173(86)90004-2.
Darriba, D., Taboada, G.L., Doallo, R., Posada, D., 2011. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164-1165. https://doi.org/10.1093/bioinformatics/btr088.
Di Tommaso, P., Moretti, S., Xenarios, I., Orobitg, M., Montanyola, A., Chang, J.-M., Taly, J.-F., Notredame, C., 2011. T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res. 39, W13-W17. https://doi.org/10.1093/nar/gkr245.
Donahue, J.L., Bownas, J.L., Niehaus, W.G., Larson, T.J., 2000. Purification and characterization of glpX-encoded fructose 1, 6-bisphosphatase, a new enzyme of the glycerol 3-phosphate regulon of Escherichia coli. J. Bacteriol. 182, 5624-5627.https://doi.org/10.1128/JB.182.19.5624-5627.2000.
Emanuelsson, O., Brunak, S., von Heijne, G., Nielsen, H., 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953-971. https://doi.org/10.1038/nprot.2007.131.
Foflonker, F., Price, D.C., Qiu, H., Palenik, B., Wang, S., Bhattacharya, D., 2015.Genome of the halotolerant green alga Picochlorum sp reveals strategies for thriving under fluctuating environmental conditions. Environ. Microbiol. 17, 412-426. https://doi.org/10.1111/1462-2920.12541.
Gao, C., Wang, Y., Shen, Y., Yan, D., He, X., Dai, J., Wu, Q., 2014. Oil accumulation mechanisms of the oleaginous microalga Chlorella protothecoides revealed through its genome, transcriptomes, and proteomes. BMC Genomics 15. https://doi.org/10.1186/1471-2164-15-582.
Haghjou, M.M., Shariati, M., Pozveh, M.H., 2006. The effect of low light intensities on oxidative stress induced by short-term chilling in Dunaliella salina teod. Pak.J. Biol. Sci. 9, 2048-2054.
Martin, W., Mustafa, A.Z., Henze, K., Schnarrenberger, C., 1996. Higher-plant chloroplast and cytosolic fructose-1,6-bisphosphatase isoenzymes: origins via duplication rather than prokaryote-eukaryote divergence. Plant Mol. Biol. 32, 485-491. https://doi.org/10.1007/bf00019100.
Merchant, S.S., Prochnik, S.E., Vallon, O., Harris, E.H., Karpowicz, S.J., Witman, G.B., Terry, A., Salamov, A., Fritz-Laylin, L.K., Maréchal-Drouard, L., 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions.Science 318, 245-250.
Notredame, C., Higgins, D.G., Heringa, J., 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217. https://doi.org/10.1006/jmbi.2000.4042.
Ogawa, T., Kimura, A., Sakuyama, H., Tamoi, M., Ishikawa, T., Shigeoka, S., 2015.Characterization and physiological role of two types of chloroplastic fructose-1,6-bisphosphatases in Euglena gracilis. Arch. Biochem. Biophys. 575, 61-68.https://doi.org/10.1016/j.abb.2015.04.002.
Polle, J.E.W., Barry, K., Cushman, J., Schmutz, J., Tran, D., Hathwaik, L.T., Yim, W.C., Jenkins, J., McKie-Krisberg, Z., Prochnik, S., Lindquist, E., Dockter, R.B., Adam, C., Molina, H., Bunkenborg, J., Jin, E., Buchheim, M., Magnuson, J., 2017. Draft nuclear genome sequence of the halophilic and beta-carotene-accumulating green alga Dunaliella salina strain CCAP19/18. Genome Announc. 5 https://doi.org/10.1128/genomeA.01105-17.
Rashid, N., Imanaka, H., Kanai, T., Fukui, T., Atomi, H., Imanaka, T., 2002. A novel candidate for the true fructose-1, 6-bisphosphatase in archaea. J. Biol. Chem. 277, 30649-30655. https://doi.org/10.1074/jbc.M202868200.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A., Huelsenbeck, J.P., 2012. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space.
Syst. Biol. 61, 539-542. https://doi.org/10.1093/sysbio/sys029.
Schoenknecht, G., Chen, W.-H., Ternes, C.M., Barbier, G.G., Shrestha, R.P., Stanke, M., Braeutigam, A., Baker, B.J., Banfield, J.F., Garavito, R.M., Carr, K., Wilkerson, C., Rensing, S.A., Gagneul, D., Dickenson, N.E., Oesterhelt, C., Lercher, M.J., Weber, A.P.M., 2013. Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339, 1207-1210. https://doi.org/10.1126/science.1231707.
Serrato, A., Maria Yubero-Serrano, E., Maria Sandalio, L., Munoz-Blanco, J., Chueca, A., Luis Caballero, J., Sahrawy, M., 2009. cpFBPaseII, a novel redoxindependent chloroplastic isoform of fructose-1,6-bisphosphatase. Plant Cell Environ. 32, 811-827. https://doi.org/10.1111/j.1365-3040.2009.01960.x.
Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690. https://doi.org/10.1093/bioinformatics/btl446.
Teich, R., Zauner, S., Baurain, D., Brinkmann, H., Petersen, J., 2007. Origin and distribution of Calvin cycle fructose and sedoheptulose bisphosphatases in plantae and complex algae: a single secondary origin of complex red plastids and subsequent propagation via tertiary endosymbioses. Protist 158, 263-276.https://doi.org/10.1016/j.protis.2006.12.004.
Verhees, C.H., Kengen, S.W.M., Tuininga, J.E., Schut, G.J., Adams, M.W.W., De Vos, W.M., Van der Oost, J., 2003. The unique features of glycolytic pathways in Archaea. Biochem. J. 375, 231-246. https://doi.org/10.1042/bj20021472.
Ye, Q., Tian, H., Chen, B., Shao, J., Qin, Y., Wen, J., 2017. Giardia's primitive GPL biosynthesis pathways with parasitic adaptation ‘patches’: implications for Giardia's evolutionary history and for finding targets against Giardiasis. Sci. Rep. 7 https://doi.org/10.1038/s41598-017-10054-1.
Zimmermann, G., Kelly, G.J., Latzko, E., 1978. Purification and properties of spinach leaf cytoplasmic fructose-1,6-bisphosphatase. J. Biol. Chem. 253, 5952-5956.

[1]	Na Su, Richard G.J. Hodel, Xi Wang, Jun-Ru Wang, Si-Yu Xie, Chao-Xia Gui, Ling Zhang, Zhao-Yang Chang, Liang Zhao, Daniel Potter, Jun Wen. Molecular phylogeny and inflorescence evolution of Prunus (Rosaceae) based on RAD-seq and genome skimming analyses[J]. Plant Diversity, 2023, 45(04): 397-408.
[2]	Yu-Feng Gu, Jiang-Ping Shu, Yi-Jun Lu, Hui Shen, Wen Shao, Yan Zhou, Qi-Meng Sun, Jian-Bing Chen, Bao-Dong Liu, Yue-Hong Yan. Insights into cryptic speciation of quillworts in China[J]. Plant Diversity, 2023, 45(03): 284-301.
[3]	Hong Qian. Patterns of phylogenetic relatedness of non-native plants across the introduction-naturalization-invasion continuum in China[J]. Plant Diversity, 2023, 45(02): 169-176.
[4]	Mei-Zhen Wang, Xiao-Kai Fan, Yong-Hua Zhang, Jing Wu, Li-Mi Mao, Sheng-Lu Zhang, Min-Qi Cai, Ming-Hong Li, Zhang-Shi-Chang Zhu, Ming-Shui Zhao, Lu-Xian Liu, Kenneth M. Cameron, Pan Li. Phylogenomics and integrative taxonomy reveal two new species of Amana (Liliaceae)[J]. Plant Diversity, 2023, 45(01): 54-68.
[5]	Ting-Shen Han, Zheng-Yan Hu, Zhi-Qiang Du, Quan-Jing Zheng, Jia Liu, Thomas Mitchell-Olds, Yao-Wu Xing. Adaptive responses drive the success of polyploid yellowcresses (Rorippa, Brassicaceae) in the Hengduan Mountains, a temperate biodiversity hotspot[J]. Plant Diversity, 2022, 44(05): 455-467.
[6]	Chao Liu, Huan-Huan Chen, Li-Zhou Tang, Phyo Kay Khine, Li-Hong Han, Yu Song, Yun-Hong Tan. Plastid genome evolution of a monophyletic group in the subtribe Lauriineae (Laureae, Lauraceae)[J]. Plant Diversity, 2022, 44(04): 377-388.
[7]	Lubing Liu, Jie Yang, Min Cao, Qinghai Song. Intraspecific trait variation of woody species reduced in a savanna community, southwest China[J]. Plant Diversity, 2022, 44(02): 163-169.
[8]	Fa-Guo Wang, Ai-Hua Wang, Cheng-Ke Bai, Dong-Mei Jin, Li-Yun Nie, AJ Harris, Le Che, Juan-Juan Wang, Shi-Yu Li, Lei Xu, Hui Shen, Yu-Feng Gu, Hui Shang, Lei Duan, Xian-Chun Zhang, Hong-Feng Chen, Yue-Hong Yan. Genome size evolution of the extant lycophytes and ferns[J]. Plant Diversity, 2022, 44(02): 141-152.
[9]	Zhi-Jian Yin, Ze-Huan Wang, Norbert Kilian, Ying Liu, Hua Peng, Ming-Xu Zhao. Mojiangia oreophila (Crepidinae, Cichorieae, Asteraceae), a new species and genus from Mojiang County, SW Yunnan, China, and putative successor of the maternal Faberia ancestor[J]. Plant Diversity, 2022, 44(01): 83-93.
[10]	Guo-Qiang Zhang, Gui-Zhen Chen, Li-Jun Chen, Jun-Wen Zhai, Jie Huang, Xin-Yi Wu, Ming-He Li, Dong-Hui Peng, Wen-Hui Rao, Zhong-Jian Liu, Si-Ren Lan. Phylogenetic incongruence in Cymbidium orchids[J]. Plant Diversity, 2021, 43(06): 452-461.
[11]	Gang Yao, Bine Xue, Kun Liu, Yuling Li, Jiuxiang Huang, Junwen Zhai. Phylogenetic estimation and morphological evolution of Alsineae (Caryophyllaceae) shed new insight into the taxonomic status of the genus Pseudocerastium[J]. Plant Diversity, 2021, 43(04): 299-307.
[12]	Jun-Chu Peng, Xiang-Guang Ma, Yue-Hua Wang, Hang Sun. New insights into the evolutionary history of Megacodon: Evidence from a newly discovered species[J]. Plant Diversity, 2020, 42(03): 198-208.
[13]	Ji-Hua Wang, Yan-Fei Cai, Shi-Feng Li, Shi-Bao Zhang. Differences in leaf physiological and morphological traits between Camellia japonica and Camellia reticulata[J]. Plant Diversity, 2020, 42(03): 181-188.
[14]	Aysajan Abdusalam, Qingjun Li. Morphological plasticity and adaptation level of distylous Primula nivalis in a heterogeneous alpine environment[J]. Plant Diversity, 2018, 40(06): 284-291.
[15]	Bang Feng, Zhuliang Yang. Studies on diversity of higher fungi in Yunnan, southwestern China: A review[J]. Plant Diversity, 2018, 40(04): 165-171.

The ubiquity and coexistence of two FBPases in chloroplasts of photosynthetic eukaryotes and its evolutionary and functional implications

The ubiquity and coexistence of two FBPases in chloroplasts of photosynthetic eukaryotes and its evolutionary and functional implications

PDF (PC)

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 15

编辑推荐

Metrics

本文评价