Skip to main content
SpringerLink
Log in

ZEBRA2, encoding a carotenoid isomerase, is involved in photoprotection in rice

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

“zebra” mutants have alternating green and chlorotic crossbands on leaf blades and are widely distributed in monocotyledonous crops. Most recently, we cloned the first responsible gene from rice, ZEBRA2, which also leads to the phenotype of rice preharvest sprouting. ZEBRA2, a single-copy gene in the rice genome, encodes a carotenoid isomerase (CRTISO), the key enzyme catalyzing the conversion of cis-lycopene to all-trans lycopene. ZEBRA2 shares high identity with known CRTISOs from other species. Expression analysis via both RT-PCR and ZEBRA2-promoter-β-glucuronidase (GUS) transgenic rice indicates that ZEBRA2 is predominantly expressed in mesophyll cells of mature leaves where active photosynthesis occurs. Consistent with the alteration in agronomic traits, the zebra2 mutant exhibits decreased photosynthetic rate and chlorophyll content. Mutation of the ZEBRA2 gene results in the accumulation of all-trans-lycopene precursor, prolycopene (7Z,9Z,7′Z,9′Z tetra cis-lycopene), in dark-grown zebra2 tissues. Light-grown zebra2 mutant exhibits the characteristic “zebra” phenotype and decreased level of lutein, the xanthophyll that is essential for efficient chl triplet quenching. More severe phenotype of the zebra2 mutant under high light intensity indicates that “zebra” phenotype might be caused by photooxidative damages. We conclude that ZEBRA2 is involved in photoprotection in rice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Aluru MR, Rodermel SR (2004) Control of chloroplast redox by the IMMUTANS terminal oxidase. Physiol Plant 120:4–11

    Article  CAS  PubMed  Google Scholar 

  • Arnon D (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:15

    Article  Google Scholar 

  • Bartley GE, Scolnik PA (1995) Plant carotenoids: pigments for photoprotection, visual attraction, and human health. Plant Cell 7:1027–1038

    Article  CAS  PubMed  Google Scholar 

  • Breitenbach J, Vioque A, Sandmann G (2001) Gene sll0033 from Synechocystis 6803 encodes a carotene isomerase involved in the biosynthesis of all-E lycopene. Z Naturforsch 56:915–917

    CAS  Google Scholar 

  • Carol P, Stevenson D, Bisanz C et al (1999) Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11:57–68

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Choi Y, Voytas DF, Rodermel S (2000) Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease. Plant J 22:303–313

    Article  PubMed  Google Scholar 

  • Chen Y, Li F, Wurtzel ET (2010) Isolation and characterization of the Z-ISO gene encoding a missing component of carotenoid biosynthesis in plants. Plant Physiol 153:66–79

    Article  CAS  PubMed  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  CAS  PubMed  Google Scholar 

  • Coe EH, Hoisington DA, Neuffer MG (1987) Linkage map of corn (maize). MNL 61:116–123

    Google Scholar 

  • Conti A, Pancaldi S, Fambrini M, Michelotti V, Bonora A, Salvini M, Pugliesi C (2004) A deficiency at the gene coding for zeta-carotene desaturase characterizes the sunflower non dormant-1 mutant. Plant Cell Physiol 45:445–455

    Article  CAS  PubMed  Google Scholar 

  • Cunningham FX, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 49:557–583

    Article  CAS  PubMed  Google Scholar 

  • Dall’Osto L, Lico C, Alric J, Giuliano G, Havaux M, Bassi R (2006) Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. BMC Plant Biol 6:32

    Article  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW III (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26

    Article  Google Scholar 

  • Dong H, Deng Y, Mu J et al (2007) The Arabidopsis Spontaneous Cell Death1 gene, encoding a zeta-carotene desaturase essential for carotenoid biosynthesis, is involved in chloroplast development, photoprotection and retrograde signalling. Cell Res 17:458–470

    CAS  PubMed  Google Scholar 

  • Fang J, Chai C, Qian Q et al (2008) Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice. Plant J 54:177–189

    Article  CAS  PubMed  Google Scholar 

  • Fong F, Smith JD, Koehler DE (1983) Early events in maize seed development: 1-methyl-3-phenyl-5-(3-[trifluoromethyl]phenyl)-4-(1H)-pyridinone induction of vivipary. Plant Physiol 73:899–901

    Article  CAS  PubMed  Google Scholar 

  • Formaggio E, Cinque G, Bassi R (2001) Functional architecture of the major light-harvesting complex from higher plants. J Mol Biol 314:1157–1166

    Article  CAS  PubMed  Google Scholar 

  • Frank HA, Cogdell RJ (1996) Carotenoids in photosynthesis. Photochem Photobiol 63:257–264

    Article  CAS  PubMed  Google Scholar 

  • Fraser PD, Pinto ME, Holloway DE, Bramley PM (2000) Technical advance: application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J 24:551–558

    Article  CAS  PubMed  Google Scholar 

  • Giraudat J, Parcy F, Bertauche N et al (1994) Current advances in abscisic acid action and signalling. Plant Mol Biol 26:1557–1577

    Article  CAS  PubMed  Google Scholar 

  • Groot S, Karssen C (1992) Dormancy and germination of abscisic acid-deficient tomato seeds: studies with the sitiens mutant. Plant Physiol 99:952–958

    Article  CAS  PubMed  Google Scholar 

  • Hable WE, Oishi KK, Schumaker KS (1998) Viviparous-5 encodes phytoene desaturase, an enzyme essential for abscisic acid (ABA) accumulation and seed development in maize. Mol Gen Genet 257:167–176

    Article  CAS  PubMed  Google Scholar 

  • Havaux M (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3:147–151

    Article  Google Scholar 

  • Hayes HK (1932) Zebra crossbands. J Hered 23:415–419

    Google Scholar 

  • He R, Ding Y, Yu J, Gao W (2000) The changes of chlorophyll content and several enzyme activities in zebra-leaf rice. J Wuhan Univer (Nat Sci Ed) 46:761–765

    CAS  Google Scholar 

  • Isaacson T, Ronen G, Zamir D, Hirschberg J (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of beta-carotene and xanthophylls in plants. Plant Cell 14:333–342

    Article  CAS  PubMed  Google Scholar 

  • Isaacson T, Ohad I, Beyer P, Hirschberg J (2004) Analysis in vitro of the enzyme CRTISO establishes a poly-cis-carotenoid biosynthesis pathway in plants. Plant Physiol 136:4246–4255

    Article  CAS  PubMed  Google Scholar 

  • Janick-Buckner D, O’Neal J, Joyce E, Bucker B (2001) Genetic and biochemical analysis of the y9 gene of maize, a carotenoid biosynthetic gene. Maydica 46:41–46

    Google Scholar 

  • Jefferson RA (1989) The GUS reporter gene system. Nature 342:837–838

    Article  CAS  PubMed  Google Scholar 

  • Kadam BS, Patel SM, Kalkarni RK (1940) Consequences of in-breeding in bajra. J Hered 31:201–207

    Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  PubMed  Google Scholar 

  • Kusumi K, Komori H, Satoh H, Iba K (2000) Characterization of a zebra mutant of rice with increased susceptibility to light stress. Plant Cell Physiol 41:158–164

    CAS  PubMed  Google Scholar 

  • Leon-Kloosterziel KM, Gil MA, Ruijs GJ et al (1996) Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant J 10:655–661

    Article  CAS  PubMed  Google Scholar 

  • Li F, Murillo C, Wurtzel E (2007) Maize Y9 encodes a product essential for 15-cis-zeta-carotene isomerization. Plant Physiol 144:1181–1189

    Article  CAS  PubMed  Google Scholar 

  • Liu XQ, Bai XQ, Wang XJ, Chu CC (2007) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol 164:969–979

    Article  CAS  PubMed  Google Scholar 

  • Luo A, Qian Q, Yin H et al (2006) EUI1, encoding a putative cytochrome P450 monooxygenase, regulates internode elongation by modulating gibberellin responses in rice. Plant Cell Physiol 47:181–191

    Article  CAS  PubMed  Google Scholar 

  • Masamoto K, Wada H, Kaneko T, Takaichi S (2001) Identification of a gene required for cis-to-trans carotene isomerization in carotenogenesis of the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 42:1398–1402

    Article  CAS  PubMed  Google Scholar 

  • Masamoto K, Hisatomi S, Sakurai I, Gombos Z, Wada H (2004) Requirement of carotene isomerization for the assembly of photosystem II in Synechocystis sp. PCC 6803. Plant Cell Physiol 45:1325–1329

    Article  CAS  PubMed  Google Scholar 

  • Naested H, Holm A, Jenkins T et al (2004) Arabidopsis VARIEGATED 3 encodes a chloroplast-targeted, zinc-finger protein required for chloroplast and palisade cell development. J Cell Sci 117:4807–4818

    Article  CAS  PubMed  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359

    Article  CAS  PubMed  Google Scholar 

  • Oki S, Gu X, Kofoid KD, Liang GH (1997) A light-intensity sensitive chlorophyll mutant in sorghum. Hereditas 126:239–245

    Article  Google Scholar 

  • Park H, Kreunen SS, Cuttriss AJ, DellaPenna D, Pogson BJ (2002) Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell 14:321–332

    Article  CAS  PubMed  Google Scholar 

  • Pogson BJ, Niyogi KK, Bjorkman O, DellaPenna D (1998) Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proc Natl Acad Sci USA 95:13324–13329

    Article  CAS  PubMed  Google Scholar 

  • Qin G, Gu H, Ma L, Peng Y, Deng XW, Chen Z, Qu LJ (2007) Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in Arabidopsis by impairing chlorophyll, carotenoid, and gibberellin biosynthesis. Cell Res 17:471–482

    Article  CAS  PubMed  Google Scholar 

  • Rosso D, Ivanov AG, Fu A et al (2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis during steady-state photosynthesis. Plant Physiol 142:574–585

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto W (2003) Leaf-variegated mutations and their responsible genes in Arabidopsis thaliana. Genes. Genet Syst 78:1–9

    Article  CAS  Google Scholar 

  • Takechi K, Sodmergen Murata M, Motoyoshi F, Sakamoto W (2000) The YELLOW VARIEGATED (VAR2) locus encodes a homologue of FtsH, an ATP-dependent protease in Arabidopsis. Plant Cell Physiol 41:1334–1346

    Article  CAS  PubMed  Google Scholar 

  • Tong H, Jin Y, Liu W et al (2009) DWARF AND LOW-TILLERING, a new member of the GRAS family, plays positive roles in brassinosteroid signaling in rice. Plant J 58:803–816

    Article  CAS  PubMed  Google Scholar 

  • Welsch R, Wüst F, Bär C, Al-Babili S, Beyer P (2008) A third phytoene synthase is devoted to abiotic stress-induced abscisic acid formation in rice and defines functional diversification of phytoene synthase genes. Plant Physiol 147:367–380

    Article  CAS  PubMed  Google Scholar 

  • Werner B, Burton G (1991) Dominant zebra mutant in pearl millet. J Hered 82:68–69

    Google Scholar 

  • Wetzel CM, Jiang CZ, Meehan LJ, Voytas DF, Rodermel SR (1994) Nuclear-organelle interactions: the immutans variegation mutant of Arabidopsis is plastid autonomous and impaired in carotenoid biosynthesis. Plant J 6:161–175

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was kindly supported by grants from National Natural Science Foundation of China (30825029, 30621001, and 30871508) and Ministry of Science and Technology (2009CB118506) to C. Chu.

Author information

Authors and Affiliations

  1. State Key Laboratory of Plant Genomics and National Centre for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, No. 1 West Beichen Road, 100101, Chaoyang District, Beijing, China

    Chenglin Chai, Jun Fang, Yang Liu, Hongning Tong, Yanqing Gong, Yiqin Wang, Min Liu, Zhukuan Cheng & Chengcai Chu

  2. Yangzhou University, 650024, Yangzhou, Jiangsu Province, China

    Yang Liu & Youping Wang

  3. China National Rice Research Institute, Chinese Academy of Agricultural Sciences, 310006, Hangzhou, Zhejiang Province, China

    Qian Qian

Authors
  1. Chenglin Chai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hongning Tong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yanqing Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yiqin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Min Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Youping Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Qian Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zhukuan Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Chengcai Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chengcai Chu.

Additional information

Chenglin Chai, Jun Fang contribute equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chai, C., Fang, J., Liu, Y. et al. ZEBRA2, encoding a carotenoid isomerase, is involved in photoprotection in rice. Plant Mol Biol 75, 211–221 (2011). https://doi.org/10.1007/s11103-010-9719-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-010-9719-z

Keywords

Search

Navigation