Abstract
Main conclusion
The rice OsFAH gene functions identically to that of Arabidopsis SSCD1 encoding FAH. Loss of OsFAH causes rice sterility.
Fumarylacetoacetate hydrolase (FAH) is the last enzyme in the tyrosine (Tyr) degradation pathway that is crucial for animals. By genetic analysis of the mutant of Short-day Sensitive Cell Death 1 gene encoding Arabidopsis FAH, we first found the pathway also plays a critical role in plants (Han et al., Plant Physiol 162:1956–1964, 2013). To further understand the role of the Tyr degradation pathway in plants, we investigated a biological function of the rice FAH. Firstly, the cDNA of rice FAH gene (OsFAH) was cloned and confirmed to be able to rescue the Arabidopsis Short-day Sensitive Cell Death 1 mutant defective in the FAH. Then, we identified the OsFAH T-DNA insertion mutant and generated the OsFAH RNA interference lines, and found that loss of OsFAH results in rice sterility. Furthermore, we analyzed expression of the OsFAH gene in roots, stems, leaves and young panicles at booting stage of rice and found that its transcript level was highest in young panicles and lowest in roots. In addition, the expression analysis of β-glucuronidase driven by OsFAH promoter in transgenic Arabidopsis showed that the OsFAH promoter was highly active in aerial tissues in vegetative stage, and sepals, filaments and stigma in reproductive stage. These results suggested that FAH plays an important role in rice fertility.
Similar content being viewed by others
Abbreviations
- FAH:
-
Fumarylacetoacetate hydrolase
- GSTZ:
-
The zeta class glutathione transferases
- GUS:
-
β-Glucuronidase
- RNAi:
-
RNA interference
- SSCD1 :
-
Short-day Sensitive Cell Death 1
References
Board PG, Baker RT, Chelvanayagam G, Jermiin LS (1997) Zeta, a novel class of glutathione transferases in a range of species from plants to humans. Biochem J 328:929–935. https://doi.org/10.1042/bj3280929
Cahoon EB, Hall SE, Ripp KG, Ganzke TS, Hitz WD, Coughlan SJ (2003) Metabolic redesign of vitamin E biosynthesis in plants for tocotrienol production and increased antioxidant content. Nat Biotechnol 21:1082–1087. https://doi.org/10.1038/nbt853
Chen D, Kawarasaki Y, Nakano H, Yamane T (2003) Cloning and in vitro and in vivo expression of plant glutathione S-transferase zeta class genes. J Biosci Bioeng 95:594–600. https://doi.org/10.1016/S1389-1723(03)80168-8
Chen S, Songkumarn P, Liu J, Wang GL (2009) A versatile zero background T-vector system for gene cloning and functional genomics. Plant Physiol 150:1111–1121. https://doi.org/10.1104/pp.109.137125
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Collakova E, DellaPenna D (2003) Homogentisate phytyltransferase activity is limiting for tocopherol biosynthesis in Arabidopsis. Plant Physiol 131:632–642. https://doi.org/10.1104/pp.015222
Dixon DP, Edwards R (2006) Enzymes of tyrosine catabolism in Arabidopsis thaliana. Plant Sci 171:360–366. https://doi.org/10.1016/j.plantsci.2006.04.008
Dixon DP, Cole DJ, Edwards R (2000) Characterisation of a zeta class glutathione transferase from Arabidopsis thaliana with a putative role in tyrosine catabolism. Arch Biochem Biophys 384:407–412. https://doi.org/10.1006/abbi.2000.2125
Farré G, Sudhakar D, Naqvi S, Sandmann G, Christou P, Capell T, Zhu CF (2012) Transgenic rice grains expressing a heterologous ρ-hydroxyphenylpyruvate dioxygenase shift tocopherol synthesis from the γ to the α isoform without increasing absolute tocopherol levels. Transgenic Res 21:1093–1097. https://doi.org/10.1007/s11248-012-9601-7
Fisher AL, Page KE, Lithgow GJ, Nash L (2008) The Caenorhabditis elegans K10C2.4 gene encodes a member of the fumarylacetoacetate hydrolase family. J Biol Chem 283:9127–9135. https://doi.org/10.1074/jbc.M708341200
Grompe M, Al-Dhalimy M, Finegold M, Ou CN, Burlingame T, Kennaway NG, Soriano P (1993) Loss of fumarylacetoacetate hydrolase is responsible for the neonatal hepatic dysfunction phenotype of lethal albino mice. Genes Dev 7:2298–2307. https://doi.org/10.1101/gad.7.12a.2298
Han CY, Ren CM, Zhi TT, Zhou Z, Liu Y, Chen F, Peng W, Xie DX (2013) Disruption of fumarylacetoacetate hydrolase causes spontaneous cell death under short-day conditions in Arabidopsis. Plant Physiol 162:1956–1964. https://doi.org/10.1104/pp.113.216804
Hickey RD, Mao SA, Glorioso J, Lillegard JB, Fisher JE, Amiot B, Rinaldo P, Harding CO, Marler R, Finegold MJ, Grompe M, Nyberg SL (2014) Fumarylacetoacetate hydrolase deficient pigs are a novel large animal model of metabolic liver disease. Stem Cell Res 13:144–153. https://doi.org/10.1016/j.scr.2014.05.003
Hildebrandt TM, Nunes Nesi A, Araújo WL, Braun HP (2015) Amino acid catabolism in plants. Mol Plant 8:1563–1579. https://doi.org/10.1016/j.molp.2015.09.005
Huang LH, Hu C, Cai W, Zhu Q, Gao BD, Zhang XW, Ren CM (2018) Fumarylacetoacetate hydrolase is involved in salt stress response in Arabidopsis. Planta 248:499–511. https://doi.org/10.1007/s00425-018-2907-9
Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651. https://doi.org/10.1016/j.bbrc.2006.04.140
Jain M, Ghanashyam C, Bhattacharjee A (2010) Comprehensive expression analysis suggests overlapping and specific roles of rice glutathione S-transferase genes during development and stress responses. BMC Genom 11:73. https://doi.org/10.1186/1471-2164-11-73
Jeon JS, Lee S, Jung KH, Jun SH, Jeong DH, Lee J, Kim C, Jang S, Lee SY, Yang K, Nam JM, An K, Han MJ, Sung RJ, Choi HS, Yu JW, Choi JH, Cho SY, Cha SS, An G (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22:561–570. https://doi.org/10.1046/j.1365-313x.2000.00767.x
Jeong DH, An S, Park S, Kang HG, Park GG, Kim SR, Sim J, Kim YO, Kim MK, Kim SR, Kim J, Shin M, Jung M, An G (2006) Generation of flanking sequence-tag database for activation-tagging lines in japonica rice. Plant J 45:123–132. https://doi.org/10.1111/j.1365-313x.2005.02610.x
Lindblad B, Lindstedt S, Steen G (1977) On the enzymic defects in hereditary tyrosinemia. Proc Natl Acad Sci USA 74:4641–4645. https://doi.org/10.1073/pnas.74.10.4641
Löffelhardt W, Kindl H (1979) Conversion of 4-hydroxyphenylpyruvic acid into homogentisic acid at the thylakoid membrane of Lemna gibba. FEBS Lett 104:332–334. https://doi.org/10.1016/0014-5793(79)80845-5
Lopukhina A, Dettenberg M, Weiler EW, Holländer-Czytko H (2001) Cloning and characterization of a coronatine-regulated tyrosine aminotransferase from Arabidopsis. Plant Physiol 126:1678–1687. https://doi.org/10.1104/pp.126.4.1678
McGonigle B, Keeler SJ, Lau SM, Koeppe MK, O’Keefe DP (2000) A genomics approach to the comprehensive analysis of the glutathione S-transferase gene family in soybean and maize. Plant Physiol 124:1105–1120. https://doi.org/10.1104/pp.124.3.1105
Miki D, Shimamoto K (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol 45:490–495. https://doi.org/10.1093/pcp/pch048
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Murray MG, Thompson WF (1980) Rapid isolation of high molecular-weight plant DNA. Nucleic Acids Res 8:4321–4325. https://doi.org/10.1093/nar/8.19.4321
Raspail C, Graindorge M, Moreau Y, Crouzy S, Lefèbvre B, Robin AY, Dumas R, Matringe M (2011) 4-Hydroxyphenylpyruvate dioxygenase catalysis: identification of catalytic residues and production of a hydroxylated intermediate shared with a structurally unrelated enzyme. J Biol Chem 286:26061–26070. https://doi.org/10.1074/jbc.M111.227595
Riewe D, Koohi M, Lisec J, Pfeiffer M, Lippmann R, Schmeichel J, Willmitzer L, Altmann T (2012) A tyrosine aminotransferase involved in tocopherol synthesis in Arabidopsis. Plant J 71:850–859. https://doi.org/10.1111/j.1365-313X.2012.05035.x
Ruppert S, Kelsey G, Schedl A, Schmid E, Thies E, Schütz G (1992) Deficiency of an enzyme of tyrosine metabolism underlies altered gene expression in newborn liver of lethal albino mice. Genes Dev 6:1430–1443. https://doi.org/10.1101/gad.6.8.1430
Sang-Ic K, Andaya VC, Tai TH (2011) Cold sensitivity in rice (Oryza sativa L.) is strongly correlated with a naturally occurring I99V mutation in the multifunctional glutathione transferase isoenzyme GSTZ2. Biochem J 435:373–380. https://doi.org/10.1042/BJ20101610
Stacey MG, Cahoon RE, Nguyen HT, Cui Y, Sato S, Nguyen CT, Phoka N, Clark KM, Liang Y, Forrester J, Batek J, Do PT, Sleper DA, Clemente TE, Cahoon EB, Stacey G (2016) Identification of homogentisate dioxygenase as a target for vitamin E biofortification in oilseeds. Plant Physiol 172:1506–1518. https://doi.org/10.1104/pp.16.00941
St-Louis M, Tanguay RM (1997) Mutations in the fumarylacetoacetate hydrolase gene causing hereditary tyrosinemia type I: overview. Hum Mutat 9:291–299. https://doi.org/10.1002/(SICI)1098-1004(1997)9:4%3c291:AID-HUMU1%3e3.0.CO;2-9
Subramaniam K, Ye Z, Buechley G, Shaner G, Solomos T, Ueng PP (1999) Isolation of a Zeta class wheat glutathione S-transferase gene. Biochim Biophys Acta 1447:348–356. https://doi.org/10.1016/S0167-4781(99)00176-1
Sun MS, Hattori S, Kubo S, Awata H, Matsuda I, Endo F (2000) A mouse model of renal tubular injury of tyrosinemia type 1: development of de Toni Fanconi syndrome and apoptosis of renal tubular cells in Fah/Hpd double mutant mice. J Am Soc Nephrol 11:291–300
Sun Q, Zybailov B, Majeran W, Friso G, Olinares PD, van Wijk KJ (2009) PPDB, the plant proteomics database at Cornell. Nucleic Acids Res 37:D969–D974. https://doi.org/10.1093/nar/gkn654
Tanguay RM, Valet JP, Lescault A, Duband JL, Laberge C, Lettre F, Plante M (1990) Different molecular basis for fumarylacetoacetate hydrolase deficiency in the two clinical forms of hereditary tyrosinemia (type 1). Am J Hum Genet 47:308–316
Tsuchiya T, Nakamura I (2004) Disruption of GSTZ1 gene by large genetic alteration in Oryza glaberrima. Breed Sci 5:67–73. https://doi.org/10.1270/jsbbs.54.67
Tsuchiya T, Takesawa T, Kanzaki H, Nakamura I (2004) Genomic structure and differential expression of two tandem-arranged GSTZ genes in rice. Gene 335:141–149. https://doi.org/10.1016/j.gene.2004.03.020
Yin Z, Wang GL (2000) Evidence of multiple complex patterns of T-DNA integration into the rice genome. Theor Appl Genet 100:461–470. https://doi.org/10.1007/s001220050060
Yoo H, Widhalm JR, Qian Y, Maeda H, Cooper BR, Jannasch AS, Gonda I, Lewinsohn E, Rhodes D, Dudareva N (2013) An alternative pathway phenylalanine biosynthesis in plants cytosolic tyrosine phenylpyruvate aminotransferase. Nat Commun 4:2833. https://doi.org/10.1038/ncomms3833
Zhi TT, Zhou Z, Huang Y, Han CY, Liu Y, Zhu Q, Ren CM (2016) Sugar suppresses cell death caused by disruption of fumarylacetoacetate hydrolase in Arabidopsis. Planta 244:557–571. https://doi.org/10.1007/s00425-016-2530-6
Acknowledgements
We thank Dr Gynheung An at Pohang University of Science and Technology/Kyung Hee University for providing the rice OsFAH T-DNA insertion line PFG_3D-01883, and Dr Guoliang Wang at Ohio State University for providing pANDA vector. The study was supported by a grant from the program for key basic research of the Ministry of Science and Technology of China (2014CB160308), a grant from Education Department of Hunan (18A100), and the Open Research Fund of Key Laboratory of Indica Rice Genetics and Breeding in the Middle and Lower Reaches of Yangtze River Valley of Ministry of Agriculture in China (Hunan Rice Research Institute) (2018KLMA03).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hu, C., Huang, L., Chen, Y. et al. Fumarylacetoacetate hydrolase is required for fertility in rice. Planta 253, 122 (2021). https://doi.org/10.1007/s00425-021-03632-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-021-03632-1