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Characterization and fine mapping of the rice gene OsARVL4 regulating leaf morphology and leaf vein development

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Abstract

Leaf morphology and chlorophyll content are closely related to the photosynthetic efficiency, which would potentially contribute to crop yield. In this study, we isolated an EMS-mutagenized rice mutant displaying abaxial rolling and vein-albino leaves, and thus designated it as Osarvl4. Compared to the wild type ‘Nipponbare’, Osarvl4 mutant had abnormal development of clear cells, parenchyma cells, sclerenchymatous cells, mesophyll cells, bulliform cells and vascular bundles. As a result of the defective leaf development, the chlorophyll content and photosynthetic efficiency were significantly affected in the mutant. Genetic analysis using map-based cloning indicated that the mutation was controlled by a single recessive karyogene localized within a 44 kb region on the long arm of chromosome 4. Sequence analysis and alignment indicated that the three candidate genes in this region showed no difference at the DNA level. However, quantitative real-time PCR analysis showed that the expression of the LOC_Os04g33580 gene in the mutant was significantly lower than that of wild type, while expression of the other two candidate genes (LOC_Os04g33560 and LOC_Os04g33570) exhibited no significant difference. Therefore, we speculate that LOC_Os04g33580 might be the target gene which regulates leaf vein development and leaf morphogenesis in rice and this locus might be subject to epigenetic regulation, such as DNA methylation, Thus, our finding suggests that the OsARVL4 gene is involved in the regulation of chlorophyll content and photosynthetic efficiency in plants, and provides a genetic basis for the future study of genes related to leaf development in rice.

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Abbreviations

DNA:

Deoxyribonucleic Acid

qPCR:

Quantitative Polymerase Chain Reaction

SSR:

Simple Sequence Repeat

InDel:

Insertion/Deletion

NPB:

Nipponbare

RCCR:

Red chlorophyll catabolite reductase

References

  • Chen WF, Xu ZJ, Zhang BL (1995) Physiological bases of super high yield breeding in rice. Liao Ning Science and Technology Publishing Company, Shenyang

    Google Scholar 

  • Dong YJ, Dong WQ, Zhang XM, Shi SY, Zhang HD (1995) Genetic analysis of low-temperature-sensitive seeding-colour character in the mutant fan 5. Chin J Rice Sci 4(9):249–250 (in Chinese with an English abstract)

    Google Scholar 

  • Feng BH, Yang Y, Shi YF, Lin L, Chen J, Wei YL, Leung H, Wu JL (2013) Genetic analysis and gene mapping of light brown spotted leaf mutant in rice. Rice Sci 20(1):13–18

    Article  CAS  Google Scholar 

  • Guo T, Huang YX, Huang Y, Liu YZ, Zhang JG, Chen ZQ, Wang H (2012) Characterizations of a mutant gene hw-1(t) for green-revertible albino high tillering and dwarf in rice (Oryza sativa L.). Acta Agronomica Sinica 38(1):23–25

    Article  CAS  Google Scholar 

  • Gustafsson K (1942) The plastid development in various types of chlorophyll mutations. Hereditas 28(3–4):483–492

    Google Scholar 

  • Hibara KI, Obara M, Hayashida E, Abe M, Ishimaru T, Satoh H, Itoh JI, Nagato Y (2009) The ADAXIALIZED LEAF1 gene functions in leaf and embryonic pattern formation in rice. Dev Biol 334:345–354

    Article  CAS  PubMed  Google Scholar 

  • Hu JT, Zhang J, Li YY, Fu CY, Zheng J, Chen JB, Hu Y, Li SG (2008) Genetic analysis and mapping of a rice white midrib mutant Oswm2. Hereditas (Beijing) 31(9):1201–1206 (in Chinese with an English abstract)

    Google Scholar 

  • Hörtensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–57

    Article  PubMed  Google Scholar 

  • Jiang SK, Zhang XJ, Xu ZJ, Chen WH (2010) Comparison between QTLs for chlorophyll content and genes controlling biosythesis and degradation in japonica rice (Oryza sativa L.). Acta Agronomica Sinica 36(3):376–384

    CAS  Google Scholar 

  • Kusaba M, Ito H, Morita R, Iida S, Sato Y, Fujimoto M, Kawasaki S, Tanaka R, Hirochika H, Nishimura M, Tanaka A (2007) Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19(4):1362–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kusumi K, Mizutani A, Nishimura M, Iba K (1997) A virescent gene V1 determinates the expression timing of plastid genes for transcription/translation apparatus during early leaf development in rice. Plant J 12:1241–1250

    Article  CAS  Google Scholar 

  • Kusumi K, Sakata C, Nakamura T, Kawasaki S, Yoshimura A, Iba K (2011) A plastid protein NUS1 is essential for build-up the genetic system for early chloroplast development under cold stress conditions. Plant J 68:1039–1050

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Kim JH, Yoo ES, Lee CH, Hirochika H, An G (2005) Differential regulation of chlorophyll a oxygenasegenes in rice. Plant Mol Biol 57:805–818

    Article  CAS  PubMed  Google Scholar 

  • Li HC, Qian Q, Wang B, Li XB, Zhu LH, Xu JC (2003) Identification and chromosomal localization of rice white panicle. Chin Sci Bull 48(3):268–270 (in Chinese)

    Article  Google Scholar 

  • Li N, Chu HW, Wen TQ, Zhang DB (2007) Genetic analysis and mapping of the rice white midrib mutant Oswm. Acta Agric Shanghai 23(1):1–4 (in Chinese with an English abstract)

    Google Scholar 

  • Li L, Shi ZY, Li L, Shen GZ, Wang XQ, An LS, Zhang JL (2010) Overexpression of ACL1 (abaxially curled leaf 1) increased bulliform cells and induced abaxial curling of leaf blades in rice. Mol Plant 3(5):807–817

    Article  CAS  PubMed  Google Scholar 

  • Liu WZ, Fu YP, Hu GC, Si H, Zhu L, Wu C, Sun ZX (2007) Identification and fine mapping of a thermo-sensitive chlorophyll deficient mutant in rice (Oryza sativa L.). Planta 226:785–795

    Article  CAS  PubMed  Google Scholar 

  • Mariko KH, Kazuhiko S, Sakae K (1987) Relationship between photosynthesis and chlorophyll content during leaf senescence of rice seedlings. Plant Cell Physiol 28(7):1321–1329

    Google Scholar 

  • Morita R, Sato Y, Masuda Y, Nishimura M, Kusaba M (2009) Defect in non-yellow coloring 3, an α/β hydrolase-fold family protein, causes a stay-green phenotype during leaf senescence in rice. Plant J 59(6):940–952

    Article  CAS  PubMed  Google Scholar 

  • Ohmori Y, Toriba T, Nakamura H, Ichikawa H, Hirano HY (2011) Temporal and spatial regulation of DROOPING LEAF gene expression that promotes midrib formation in rice. Plant J 65:77–86

    Article  CAS  PubMed  Google Scholar 

  • Panaud O, Chen X, McCouch SR (1996) Development microsatellite markers characterization of simple sequence length polymorphism (SSLPs) in rice (Oryza sativa L.). Mol Gen Genet 259:597–607

    Google Scholar 

  • Qi J, Qian Q, Bu QY, Li SY, Chen Q, Sun JQ, Liang WX, Zhou YH, Chu CC, Li XG, Ren FG, Palme K, Zhao BR, Chen JF, Chen MS, Li CY (2008) Mutation of rice Narrow leaf1 gene, which encodes a novel protein, affects vein patterning and polar auxin transport. Plant Physiol 147:1947–1959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato Y, Morita R, Katsuma S, Nishimura M, Tanaka A, Kusaba M (2009) Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice. Plant J 57(1):120–131

    Article  CAS  PubMed  Google Scholar 

  • Sheng ZH, Wei XJ, Shao GN, Song J, Luo J, Hu PS, Tang SQ, Chen LY (2013) Genetic analysis and molecular mapping of novel white striped leaf mutant gene in rice. Rice Sci 20(5):336–342

    Article  Google Scholar 

  • Su N, Hu ML, Wu DX, Wu FQ, Fei GL, Lan Y, Chen XL, Shu XL, Zhang X, Guo XP, Cheng ZJ, Lei CL, Qi CK, Jiang L, Wang H, Wan JM (2012) Disruption of a rice pentatricopeptide repeat protein causes a seedling-specific albino phenotype and its utilization to enhance seed purity in hybrid rice production. Plant Physiol 159(1):227–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takai T, Adachi S, Shiobara FT, Arai YS, Iwasawa N, Yoshinaga S, Hirose S, Taniguchi Y, Yamanouchi U, Wu JZ, Matsumoto T, Sugimoto K, Kondo K, Ikka T, Ando T, Kono I, Ito S, Shomura A, Ookawa T, Hirasawa T, Yano M, Kondo M, Yamamoto T (2013) A natural variant of NAL1, selected in high-yield rice breeding programs, pleiotropically increases photosynthesis rate. Sci Rep 3:2149. doi:10.1038/srep02149

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang YY, Li MR, Chen YP, Wu PZ, Wu GJ, Jiang HW (2011) Knockdown of OsPAO and OsRCCR1 cause different plant death phenotypes in rice. J Plant Physiol 168:1952–1959

    Article  CAS  PubMed  Google Scholar 

  • Teng S, Qian Q, Zeng DL, Kunihiro Y, Fujimoto K, Huang DN, Zhu LH (2004) QTL analysis of leaf photosynthetic rate and related physiological traits in rice (Oryza sativa L.). Euphytica 135:1–7

    Article  CAS  Google Scholar 

  • Wu ZM, Zhang X, He B, Diao LP, Sheng SL, Wang JL, Guo XP, Su N, Wang LF, Jiang L, Wang CM, Zhai HQ, Wan JM (2007) A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis. Plant Physiol 145(1):29–40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu RH, Li BS, He S, Wabmann F, Yu C, Qin GJ, Schreiber L, Qu LJ, Gu HY (2011) CFL1, a WW domain protein, regulates cuticle development by modulating the function of HDG1, a class IV homeodomain transcription factor, in rice and arabidopsis. Plant Cell 23:3392–3411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu SH, Xue JJ, Zhang HY, Xu PZ, Wu XJ (2012) Special DNA methylated sites between haploid of twin-seedling and its hybrids in rice (Oryza sativa). Rice Sci 19(1):94–99

    Article  Google Scholar 

  • Xu J, Wang L, Qian Q, Zhang GH (2013) Research advance in molecule regulation mechanism of leaf morphogenesis in Rice (Oryza sativa L.). Acta Agronomica Sinica 39(5):767–774

    Article  CAS  Google Scholar 

  • Yamatani H, Sato Y, Masuda Y, Kato Y, Morita R, Fukunaga K, Nagamura Y, Nishimura M, Sakamoto W, Tanaka A, Kusaba M (2013) NYC4, the rice ortholog of Arabidopsis THF1, is involved in the degradation of chlorophyll—protein complexes during leaf senescence. Plant J 74:652–662

    Article  CAS  PubMed  Google Scholar 

  • Yan S, Yan CJ, Gu MH (2008) Molecular mechanism of leaf development. Hereditas (Beijing) 30(9):1127–1135 (in Chinese with an English abstract)

    Article  CAS  Google Scholar 

  • Zhang HT, Li JJ, Yoo JH, Yoo SC, Cho SH, Koh HJ, Seo HS, Paek NC (2006) Rice Chlorina-1 and Chlorina-9 encode ChlD and ChlI subunits of Mg-chelatase, a key enzyme for chlorophyll synthesis and chloroplast development. Plant Mol Biol 62:325–337

    Article  CAS  PubMed  Google Scholar 

  • Zhang GH, Xu Q, Zhu XD, Qian Q, Xue HW (2009) SHALLOT-LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. Plant Cell 21:719–735

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang LG, Cheng ZJ, Qin RZ, Qiu Y, Wang JL, Cui XK, Gu LF, Zhang X, Guo XP, Wang D, Jiang L, Wu CY, Wang HY, Cao XF, Wan JM (2012) Identification and Characterization of an Epi-Allele of FIE1 reveals a regulatory linkage between two epigenetic marks in rice. Plant Cell 24(11):4407–4421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao SQ, Hu J, Guo LB, Qian Q, Xue HW (2010) Rice leaf inclination2, a VIN3-like protein, regulates leaf angle through modulating cell division of the collar. Cell Res 20:935–947

    Article  CAS  PubMed  Google Scholar 

  • Zhao CF, Xu JM, Chen Y, Mao CZ, Zhang SL, Bai YH, Jiang D, Wu P (2012) Molecular cloning and characterization of OsCHR4, a rice chromatin-remodeling factor required for early chloroplast development in adaxial mesophyll. Planta 236:1165–1176

    Article  CAS  PubMed  Google Scholar 

  • Zou LP, Peng M (2013) Research progress on rice blade veins development. J Agric Sci Technol Iran 15(1):43–47

    Google Scholar 

  • Zou LP, Sun XH, Zhang ZG, Liu P, Wu JX, Tian CJ, Qiu JL, Lu TG (2011) Leaf rolling controlled by the homeodomain Leucine Zipper Class IV gene Roc5 in rice. Plant Physiol 156:1589–1602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (91335105, 31201194 and 31171531); Provincial Science Fund for Distinguished Young Scholars of Zhejiang (R3100100).

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Correspondence to Qian Qian or Guangheng Zhang.

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Li Wang and Jing Xu have contributed equally to this work.

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Wang, L., Xu, J., Nian, J. et al. Characterization and fine mapping of the rice gene OsARVL4 regulating leaf morphology and leaf vein development. Plant Growth Regul 78, 345–356 (2016). https://doi.org/10.1007/s10725-015-0097-z

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  • DOI: https://doi.org/10.1007/s10725-015-0097-z

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