Plant Growth Regulation

, Volume 85, Issue 1, pp 1–13 | Cite as

Photosynthesis, cellulose contents and ultrastructure changes of mutant rice leading to screw flag leaf

  • Md. Alamin
  • Dong-Dong Zeng
  • Most. Humaira Sultana
  • Ran Qin
  • Xiao-Li Jin
  • Chun-Hai Shi
Original paper


Leaf rolling is one of the most commonly observed phenotypes in plants and recently more concentration has been paid by researchers on the rolling leaf mutants because of the abundance of rolling leaf phenotypes in rice. The photosynthesis efficiency, chlorophyll contents, cellulose contents, chlorophyll fluorescence and ultrastructure changes between screw flag leaf 1 (sfl1) mutant found in Zhenong 34 (Oryza sativa L. ssp. indica) and wild type (WT) were investigated in the present study. The results indicated that the net photosynthesis rate, stomata conductance, intercellular CO2 concentration and transpiration rate in sfl1 were significantly lower than those in WT. Compared with the WT plant, the chlorophyll a, chlorophyll a + b, Chl a/b and carotenoid contents in sfl1 were significantly decreased, however, the chlorophyll b was lower in WT. The results of chlorophyll fluorescence showed that the variations in maximal quantum yield of PSII (Fv/Fm), effective quantum yield of PSII (ΦPSII) and electron transfer rate (ETR) in sfl1 mutant flag leaves were visibly decreased but photochemical quenching coefficient (qP) and non photochemical quenching coefficient (NPQ) were increased compared with those in the WT. We demonstrated that the cellulose and hemicelluloses contents in sfl1 were significantly lower than those in the WT, while the lignin content was significantly increased in sfl1. Transmission electron micrographs (TEM) revealed that there were distinguishing differences in the chloroplast, mitochondria and starch grana between sfl1 and WT at vegetative stage. However, there was no observable thylakoid in sfl1 chloroplasts at the reproductive stage, indicating that the chloroplasts could be largely undifferentiated in this mutant. These results might provide the significant basis for further understanding the screw leaf development mechanism in rice.


Rice (Oryza sativa L.) Screw flag leaf Transmission electron micrographs (TEM) Photosynthesis Cellulose 



This work was supported by the Science and Technology Office of Zhejiang Province (2012C12901-2 and 2016C32G2010016), Program for Innovative Research Team in University (IRT1185) and the Ministry of Education and Bureau of Foreign Experts of China (Grant B14027). We are thankful to Jocelyn Mikel Losh (College of Life Sciences, Zhejiang University) for her critical review.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10725_2018_369_MOESM1_ESM.doc (70 kb)
Supplementary material 1 (DOC 70 KB)


  1. Adachi S, Yoshikawa K, Yamanouchi U, Tanabata T, Sun J, Ookawa T, Yamamoto T, Sage RF, Hirasawa T, Yonemaru J (2017) Fine mapping of Carbon Assimilation Rate 8, a quantitative trait locus for flag leaf nitrogen content, stomatal conductance and photosynthesis in rice. Front Plant Sci 8:60. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ahammed GJ, Ruan YP, Zhou J, Xia XJ, Shi K, Zhou YH, Yu JQ (2013) Brassinosteroid alleviates polychlorinated biphenyls-induced oxidative stress by enhancing antioxidant enzymes activity in tomato. Chemosphere 90(11):2645–2653. CrossRefPubMedGoogle Scholar
  3. Ahmed IM, Cao F, Zhang M, Chen X, Zhang G, Wu F (2013) Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys. PLoS ONE 8(10):e77869. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Alamin M, Zeng DD, Qin R, Sultana MH, Jin XL, Shi CH (2017) Characterization and fine mapping of SFL1, a gene controlling Screw Flag Leaf in rice. Plant Mol Biol Rep 35(5):491–503. CrossRefGoogle Scholar
  5. Ambavaram MM, Krishnan A, Trijatmiko KR, Pereira A (2011) Coordinated activation of cellulose and repression of lignin biosynthesis pathways in rice. Plant Physiol 155(2):916–931. CrossRefPubMedGoogle Scholar
  6. Arnon DI (1949) Copper enzymes in isolated chloroplasts. polyphenoloxidase in beta vulgaris. Plant Physiol 24(1):1–15CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bai L, Duan ZQ, Wang JM, An LZ, Zhao ZG, Chen KM (2008) Anatomical and chemical characteristics of a rolling leaf mutant of rice and its ecophysiological properties. Rice Sci 15(3):201–208. CrossRefGoogle Scholar
  8. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546. CrossRefPubMedGoogle Scholar
  9. Boex-Fontvieille E, Davanture M, Jossier M, Zivy M, Hodges M, Tcherkez G (2014) Photosynthetic activity influences cellulose biosynthesis and phosphorylation of proteins involved therein in Arabidopsis leaves. J Exp Bot 65(17):4997–5010. CrossRefPubMedGoogle Scholar
  10. Candela H, Johnston R, Gerhold A, Foster T, Hake S (2008) The milkweed pod1 gene encodes a KANADI protein that is required for abaxial/adaxial patterning in maize leaves. Plant Cell 20(8):2073–2087. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chang YC, Walling LL (1992) Spatial and temporal expression of Cab mRNAs in cotyledons of the developing soybean seedling. Planta 186(2):262–272. CrossRefPubMedGoogle Scholar
  12. Chen Q, Xie Q, Gao J, Wang W, Sun B, Liu B, Zhu H, Peng H, Zhao H, Liu C, Wang J, Zhang J, Zhang G, Zhang Z (2015) Characterization of Rolled and Erect Leaf 1 in regulating leave morphology in rice. J Exp Bot 66(19):6047–6058. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Clarke JM (1986) Effect of leaf rolling on leaf water-loss in Triticum Spp. Can J Plant Sci 66(4):885–891. CrossRefGoogle Scholar
  14. Di D-W, Zhang C, Luo P, An C-W, Guo G-Q (2016) The biosynthesis of auxin: how many paths truly lead to IAA? Plant Growth Regul 78(3):275–285. CrossRefGoogle Scholar
  15. Driever SM, Lawson T, Andralojc PJ, Raines CA, Parry MAJ (2014) Natural variation in photosynthetic capacity, growth, and yield in 64 field-grown wheat genotypes. J Exp Bot 65(17):4959–4973. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Fahad S, Hussain S, Matloob A, Khan FA, Khaliq A, Saud S, Hassan S, Shan D, Khan F, Ullah N, Faiq M, Khan MR, Tareen AK, Khan A, Ullah A, Ullah N, Huang J (2015) Phytohormones and plant responses to salinity stress: a review. Plant Growth Regul 75(2):391–404. CrossRefGoogle Scholar
  17. Fang L, Zhao F, Cong Y, Sang X, Du Q, Wang D, Li Y, Ling Y, Yang Z, He G (2012) Rolling-leaf14 is a 2OG-Fe(II) oxygenase family protein that modulates rice leaf rolling by affecting secondary cell wall formation in leaves. Plant Biotechnol J 10(5):524–532. CrossRefPubMedGoogle Scholar
  18. Fujino K, Matsuda Y, Ozawa K, Nishimura T, Koshiba T, Fraaije MW, Sekiguchi H (2008) NARROW LEAF 7 controls leaf shape mediated by auxin in rice. Mol Genet Genom 279(5):499–507. CrossRefGoogle Scholar
  19. Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327(5967):812–818. CrossRefPubMedGoogle Scholar
  20. Horton P (2000) Prospects for crop improvement through the genetic manipulation of photosynthesis: morphological and biochemical aspects of light capture. J Exp Bot 51:475–485. CrossRefPubMedGoogle Scholar
  21. Joshi CP, Mansfield SD (2007) The cellulose paradox—simple molecule, complex biosynthesis. Curr Opin Plant Biol 10(3):220–226. CrossRefPubMedGoogle Scholar
  22. Kadioglu A, Terzi R (2007) A dehydration avoidance mechanism: leaf rolling. Bot Rev 73(4):290–302CrossRefGoogle Scholar
  23. Kadioglu A, Terzi R, Saruhan N, Saglam A (2012) Current advances in the investigation of leaf rolling caused by biotic and abiotic stress factors. Plant Sci 182:42–48. CrossRefPubMedGoogle Scholar
  24. Khush GS (2013) Strategies for increasing the yield potential of cereals: case of rice as an example. Plant Breed 132(5):433–436. Google Scholar
  25. Lang Y, Zhang Z, Gu X, Yang J, Zhu Q (2004) Physiological and ecological effects of crimpy leaf character in rice (Oryza saliva L.) II. photosynthetic character, dry mass production and yield forming. Zuo Wu Bao 30:883–887Google Scholar
  26. Li M, Xiong G, Li R, Cui J, Tang D, Zhang B, Pauly M, Cheng Z, Zhou Y (2009) Rice cellulose synthase-like D4 is essential for normal cell-wall biosynthesis and plant growth. Plant J 60(6):1055–1069. CrossRefPubMedGoogle Scholar
  27. Lima Neto MC, Lobo AK, Martins MO, Fontenele AV, Silveira JA (2014) Dissipation of excess photosynthetic energy contributes to salinity tolerance: a comparative study of salt-tolerant Ricinus communis and salt-sensitive Jatropha curcas. J Plant Physiol 171(1):23–30. CrossRefPubMedGoogle Scholar
  28. Luan W, Liu Y, Zhang F, Song Y, Wang Z, Peng Y, Sun Z (2011) OsCD1 encodes a putative member of the cellulose synthase-like D sub-family and is essential for rice plant archeitecture and growth. Plant Bio J 9(4):513–524. CrossRefGoogle Scholar
  29. Malinowski R (2013) Understanding of leaf development-the science of complexity. Plants (Basel) 2(3):396–415. CrossRefGoogle Scholar
  30. Micol JL, Hake S (2003) The development of plant leaves. Plant Physiol 131(2):389–394. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Murchie EH, Pinto M, Horton P (2009) Agriculture and the new challenges for photosynthesis research. New Phytol 181(3):532–552. CrossRefPubMedGoogle Scholar
  32. Nelson JM, Lane B, Freeling M (2002) Expression of a mutant maize gene in the ventral leaf epidermis is sufficient to signal a switch of the leaf’s dorsoventral axis. Development 129:4581–4589PubMedGoogle Scholar
  33. Ohsumi A, Hamasaki A, Nakagawa H, Yoshida H, Shiraiwa T, Horie T (2007) A model explaining genotypic and ontogenetic variation of leaf photosynthetic rate in rice (Oryza sativa) based on leaf nitrogen content and stomatal conductance. Ann Bot 99(2):265–273. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Persson S, Caffall KH, Freshour G, Hilley MT, Bauer S, Poindexter P, Hahn MG, Mohnen D, Somerville C (2007) The Arabidopsis irregular xylem8 mutant is deficient in glucuronoxylan and homogalacturonan, which are essential for secondary cell wall integrity. Plant Cell 19(1):237–255. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Price AH, Young EM, Tomos AD (1997) Quantitative trait loci associated with stomatal conductance, leaf rolling and heading date mapped in upland rice (Oryza sativa). New Phytol 137(1):83–91. CrossRefGoogle Scholar
  36. Saruhan N, Terzi R, Saglam A, Kadioglu A (2010) Scavenging of reactive oxygen species in apoplastic and symplastic areas of rolled leaves in Ctenanthe setosa under drought stress. Acta Biol Hung 61(3):282–298. CrossRefPubMedGoogle Scholar
  37. Tang Y, Wen X, Lu Q, Yang Z, Cheng Z, Lu C (2007) Heat stress induces an aggregation of the light-harvesting complex of photosystem II in spinach plants. Plant Physiol 143(2):629–638. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Tanimoto T, Itoh R (2000) Effect of leaf rolling on transpiration and water use efficiency in rice. Jpn J Crop Sci 69(3):406–412. CrossRefGoogle Scholar
  39. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7(11):847–859. CrossRefPubMedGoogle Scholar
  40. Teng S, Qian Q, Zeng D, Kunihiro Y, Fujimoto K, Huang D, Zhu L (2004) QTL analysis of leaf photosynthetic rate and related physiological traits in rice (Oryza sativa L.). Euphytica 135(1):1–7. CrossRefGoogle Scholar
  41. Tsuda K, Ito Y, Yamaki S, Miyao A, Hirochika H, Kurata N (2009) Isolation and mapping of three rice mutants that showed ectopic expression of KNOX genes in leaves. Plant Sci 177(2):131–135. CrossRefGoogle Scholar
  42. Tsuda K, Akiba T, Kimura F, Ishibashi M, Moriya C, Nakagawa K, Kurata N, Ito Y (2013) ONION2 fatty acid elongase is required for shoot development in rice. Plant Cell Physiol 54(2):209–217. CrossRefPubMedGoogle Scholar
  43. Tsutsumi K, Taniguchi Y, Kawasaki M, Taniguchi M, Miyake H (2006) Expression of photosynthesis-related genes during the leaf development of a C3 plant rice as visualized by in situ hybridization. Plant Prod Sci 9(3):232–241. CrossRefGoogle Scholar
  44. Vansoest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74(10):3583–3597. CrossRefGoogle Scholar
  45. Wang L, Xu J, Nian J, Shen N, Lai K, Hu J, Zeng D, Ge C, Fang Y, Zhu L, Qian Q, Zhang G (2016) Characterization and fine mapping of the rice gene OsARVL4 regulating leaf morphology and leaf vein development. Plant Growth Regul 78(3):345–356. CrossRefGoogle Scholar
  46. Wu XJ (2009) Prospects of developing hybrid rice with super high yield. Agron J 101(3):688–695. CrossRefGoogle Scholar
  47. Xiang JJ, Zhang GH, Qian Q, Xue HW (2012) SEMI-ROLLED LEAF1 encodes a putative glycosylphosphatidylinositol-anchored protein and modulates rice leaf rolling by regulating the formation of bulliform cells. Plant Physiol 159(4):1488–1500. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Xiao Y, Tholen D, Zhu XG (2016) The influence of leaf anatomy on the internal light environment and photosynthetic electron transport rate: exploration with a new leaf ray tracing model. J Exp Bot 67(21):6021–6035. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Xing Y, Zhang Q (2010) Genetic and molecular bases of rice yield. Annu Rev Plant Biol 61:421–442. CrossRefPubMedGoogle Scholar
  50. Yang EN, Yang ZJ, Zhang JF, Zou YC, Ren ZL (2011) Molecular cytogenetic characterization of a new leaf rolling triticale. Genet Mol Res 10(4):2953–2961. CrossRefPubMedGoogle Scholar
  51. Yang C, Li D, Liu X, Ji C, Hao L, Zhao X, Li X, Chen C, Cheng Z, Zhu L (2014) OsMYB103L, an R2R3-MYB transcription factor, influences leaf rolling and mechanical strength in rice (Oryza sativa L.). BMC Plant Biol 14:158. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Yang Y-L, Xu J, Rao Y-C, Zeng Y-J, Liu H-J, Zheng T-T, Zhang G-H, Hu J, Guo L-B, Qian Q, Zeng D-L, Shi Q-H (2016) Cloning and functional analysis of pale-green leaf (PGL10) in rice (Oryza sativa L.). Plant Growth Regul 78(1):69–77. CrossRefGoogle Scholar
  53. Ye W, Hu S, Wu L, Ge C, Cui Y, Chen P, Xu J, Dong G, Guo L, Qian Q (2017) Fine mapping a major QTL qFCC7L for chlorophyll content in rice (Oryza sativa L.) cv. PA64s. Plant Growth Regul 81(1):81–90. CrossRefGoogle Scholar
  54. Yu H, Qiu Z, Xu Q, Wang Z, Zeng D, Hu J, Zhang G, Zhu L, Gao Z, Chen G, Guo L, Qian Q, Ren D (2017) Fine mapping of LOW TILLER 1, a gene controlling tillering and panicle branching in rice. Plant Growth Regul 83(1):93–104. CrossRefGoogle Scholar
  55. 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(3):719–735. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Zhang J, Nallamilli BR, Mujahid H, Peng Z (2010) OsMADS6 plays an essential role in endosperm nutrient accumulation and is subject to epigenetic regulation in rice (Oryza sativa). Plant J 64(4):604–617. CrossRefPubMedGoogle Scholar
  57. Zhang JJ, Wu SY, Jiang L, Wang JL, Zhang X, Guo XP, Wu CY, Wan JM (2015) A detailed analysis of the leaf rolling mutant sll2 reveals complex nature in regulation of bulliform cell development in rice (Oryza sativa L.). Plant Biol 17(2):437–448. CrossRefPubMedGoogle Scholar
  58. 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. CrossRefPubMedGoogle Scholar
  59. Zhao X, Chen T, Feng B, Zhang C, Peng S, Zhang X, Fu G, Tao L (2016) Non-photochemical quenching plays a key role in light acclimation of rice plants differing in leaf color. Front Plant Sci 7:1968. PubMedGoogle Scholar
  60. Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20(10):2763–2782. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Md. Alamin
    • 1
  • Dong-Dong Zeng
    • 1
  • Most. Humaira Sultana
    • 1
  • Ran Qin
    • 1
  • Xiao-Li Jin
    • 1
  • Chun-Hai Shi
    • 1
  1. 1.Department of AgronomyZhejiang UniversityHangzhouChina

Personalised recommendations