Advertisement

Plant Cell Reports

, Volume 38, Issue 12, pp 1473–1484 | Cite as

A maize NAC transcription factor, ZmNAC34, negatively regulates starch synthesis in rice

  • Xiaojian PengEmail author
  • Qianqian Wang
  • Yu Wang
  • Beijiu Cheng
  • Yang Zhao
  • Suwen ZhuEmail author
Original Article

Abstract

Key message

ZmNAC34 might function as an important regulator of starch synthesis by decreasing total starch accumulation and soluble sugar content and increasing amylose fractions.

Abstract

Starch is a major component in endosperm and directly influences seed yield and the cooking quality of cereal grains. Starch is synthesized through a series of complex biological processes. Nevertheless, the mechanism by which starch biosynthesis is regulated in maize is still unclear. In this study, ZmNAC34, a NAC transcription factor related to starch synthesis, was screened based on transcriptome sequencing data. Subsequent qRT-PCR analysis showed that ZmNAC34 is specifically expressed in maize endosperm. Transactivation and subcellular localization assays revealed that ZmNAC34 possesses two characteristics of transcription factors: nuclear localization and transactivation activity. Overexpression of ZmNAC34 in rice decreased total starch accumulation and soluble sugar content, while increased amylose fractions. Meanwhile, the transgenic seeds exhibited alterant starch structure and abnormal morphology. In addition, compared with WT seeds, most of the 17 starch biosynthesis-related genes were significantly upregulated in transgenic seeds from 6 to 15 DAP (day after pollination). These data reveal that ZmNAC34 might function as an important regulator of starch synthesis, thus providing a new perspective on controlling seed yield and quality.

Keywords

Maize ZmNAC34 Endosperm Starch synthesis 

Notes

Acknowledgements

We thank members of National Engineering Laboratory of Crop Stress Resistance Breeding for their suggestions in my experimental design and data processing. Funding was provided by Natural Science Foundation of Anhui Province to Xiaojian Peng and Qianqian Wang (Grant numbers 1908085QC133 and 1908085QC134).

Author contribution statement

SZ and XP conceived the project. QW and YW carried out the experiments and YZ performed the statistical analysis. BC, SZ and XP wrote the manuscript. All authors read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

299_2019_2458_MOESM1_ESM.tif (708 kb)
Supplementary material 1 (TIFF 708 kb): The coding sequence and amino acid sequence of ZmNAC34
299_2019_2458_MOESM2_ESM.tif (2.5 mb)
Supplementary material 2 (TIFF 2605 kb): The positive transgenic seeds were detected by GUS staining method
299_2019_2458_MOESM3_ESM.tif (472 kb)
Supplementary material 3 (TIFF 472 kb): ZmNAC34-overexpression transgenic plants were detected through PCR assays
299_2019_2458_MOESM4_ESM.tif (82 kb)
Supplementary material 4 (TIFF 82 kb): Expression level of ZmNAC34 in transgenic seeds
299_2019_2458_MOESM5_ESM.doc (40 kb)
Supplementary material 5 (DOC 40 kb)

References

  1. Ball SG, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annu Rev Plant Biol 54(1):207–233CrossRefGoogle Scholar
  2. Brummell DA, Watson LM, Zhou J, McKenzie MJ, Hallett IC, Simmons L, Carpenter M, Timmerman-Vaughan GM (2015) Overexpression of starch branching enzyme II increases short-chain branching of amylopectin and alters the physicochemical properties of starch from potato tuber. BMC Biotechnol 15:28.  https://doi.org/10.1186/s12896-015-0143-y PubMedPubMedCentralCrossRefGoogle Scholar
  3. Cai H, Chen Y, Zhang M, Cai R, Cheng B, Ma Q, Zhao Y (2017) A novel GRAS transcription factor, ZmGRAS20, regulates starch biosynthesis in rice endosperm. Physiol Mol Biol Plants 23(1):1–12CrossRefGoogle Scholar
  4. Cano A, Jiménez A, Cháfer M, Gónzalez C, Chiralt A (2014) Effect of amylose: amylopectin ratio and rice bran addition on starch films properties. Carbohyd Polym 111:543–555CrossRefGoogle Scholar
  5. Chen J, Yi Q, Cao Y, Wei B, Zheng LJ, Xiao QL, Xie Y, Gu Y, Li YP, Huang HH, Wang YB, Hou XB, Long TD, Zhang JJ, Liu HM, Liu YH, Yu GW, Huang YB (2016) ZmbZIP91 regulates expression of starch synthesis-related genes by binding to ACTCAT elements in their promoters. J Exp Bot 67(5):1327–1338.  https://doi.org/10.1093/jxb/erv527 PubMedCrossRefGoogle Scholar
  6. Denyer K, Johnson P, Zeeman S, Smith AM (2001) The control of amylose synthesis. J Plant Physiol 158(4):479–487CrossRefGoogle Scholar
  7. Dickinson DB, Preiss J (1969) Presence of ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize endosperm. Plant Physiol 44(7):1058–1062PubMedPubMedCentralCrossRefGoogle Scholar
  8. Doan DN, Rudi H, Olsen OA (1999) The allosterically unregulated isoform of ADP-glucose pyrophosphorylase from barley endosperm is the most likely source of ADP-glucose incorporated into endosperm starch. Plant Physiol 121(3):965–975PubMedPubMedCentralCrossRefGoogle Scholar
  9. Duval M, Hsieh TF, Kim SY, Thomas TL (2002) Molecular characterization of AtNAM: a member of the arabidopsis NAC domain superfamily. Plant Mol Biol 50(2):237–248PubMedCrossRefGoogle Scholar
  10. Fisher DK, Boyer CD, Hannah LC (1993) Starch branching enzyme II from maize endosperm. Plant Physiol 102(3):1045PubMedPubMedCentralCrossRefGoogle Scholar
  11. Fu FF, Xue HW (2010) Coexpression analysis identifies rice starch regulator1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol 154(2):927–938PubMedPubMedCentralCrossRefGoogle Scholar
  12. Gilbert G, Spragg S (1964) Iodimetric determination of amylose. Methods Carbohydr Chem 4:168–169Google Scholar
  13. He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44(6):903–916PubMedCrossRefGoogle Scholar
  14. Hirose T, Terao T (2004) A comprehensive expression analysis of the starch synthase gene family in rice (Oryza sativa L.). Planta 220(1):9–16PubMedCrossRefGoogle Scholar
  15. Hizukuri S (1986) Polymodal distribution of the chain lengths of amylopectins, and its significance. Carbohyd Res 147(2):342–347CrossRefGoogle Scholar
  16. Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci 103(35):12987–12992PubMedCrossRefGoogle Scholar
  17. Hu YF, Li YP, Zhang J, Liu H, Chen Z, Huang Y (2011) PzsS3a, a novel endosperm specific promoter from maize (Zea mays L.) induced by ABA. Biotechnol Lett 33(7):1465–1471PubMedCrossRefGoogle Scholar
  18. Hu YF, Li YP, Zhang J, Liu H, Tian M, Huang Y (2012) Binding of ABI4 to a CACCG motif mediates the ABA-induced expression of the ZmSSI gene in maize (Zea mays L.) endosperm. J Exp Bot 63(16):5979–5989PubMedCrossRefGoogle Scholar
  19. James MG, Denyer K, Myers AM (2003) Starch synthesis in the cereal endosperm. Curr Opin Plant Biol 6(3):215–222.  https://doi.org/10.1016/S1369-5266(03)00042-6 PubMedCrossRefGoogle Scholar
  20. Jeon JS, Ryoo N, Hahn TR, Walia H, Nakamura Y (2010) Starch biosynthesis in cereal endosperm. Plant Physiol Biochem 48(6):383–392.  https://doi.org/10.1016/j.plaphy.2010.03.006 CrossRefGoogle Scholar
  21. Jiang Y, Zeng B, Zhao H, Zhang M, Xie S, Lai J (2012) Genome-wide transcription factor gene prediction and their expressional tissue-specificities in maize. J Integr Plant Biol 54(9):616–630PubMedCrossRefGoogle Scholar
  22. Juliano B (1998) Varietal impact on rice quality. Cereal Foods World 43(4):207–222Google Scholar
  23. Kang GZ, Xu W, Liu GQ, Peng XQ, Guo TC (2012) Comprehensive analysis of the transcription of starch synthesis genes and the transcription factor RSR1 in wheat (Triticum aestivum) endosperm. Genome 56(2):115–122PubMedCrossRefGoogle Scholar
  24. Lai J, Dey N, Kim CS, Bharti AK, Rudd S, Mayer KF, Larkins BA, Becraft P, Messing J (2004) Characterization of the maize endosperm transcriptome and its comparison to the rice genome. Genome Res 14(10a):1932–1937PubMedPubMedCentralCrossRefGoogle Scholar
  25. Liu YY, Li JZ, Li YL, Wei MG, Cui QX, Wang QL (2010) Identification of differentially expressed genes at two key endosperm development stages using two maize inbreds with large and small grain and integration with detected QTL for grain weight. Theor Appl Genet 121(3):433–447.  https://doi.org/10.1007/s00122-010-1321-x PubMedCrossRefGoogle Scholar
  26. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−ΔΔC(T)) method. Methods 25(4):402–408CrossRefGoogle Scholar
  27. Mafongoya P, Rusinamhodzi L, Siziba S, Thierfelder C, Mvumi BM, Nhau B, Hove L, Chivenge P (2016) Maize productivity and profitability in conservation agriculture systems across agro-ecological regions in Zimbabwe: a review of knowledge and practice. Agr Ecosyst Environ 220:211–225.  https://doi.org/10.1016/j.agee.2016.01.017 CrossRefGoogle Scholar
  28. Myers AM, Morell MK, James MG, Ball SG (2000) Recent progress toward understanding biosynthesis of the amylopectin crystal. Plant Physiol 122(4):989–998PubMedPubMedCentralCrossRefGoogle Scholar
  29. Nakamura T, Yamamori M, Hirano H, Hidaka S, Nagamine T (1995) Production of waxy (amylose-free) wheats. Mol Gen Genet 248(3):253–259PubMedCrossRefGoogle Scholar
  30. Nelson O, Pan D (1995) Starch synthesis in maize endosperms. Annu Rev Plant Physiol Plant Mol Biol 46(1):475–496.  https://doi.org/10.1146/annurev.pp.46.060195.002355 CrossRefGoogle Scholar
  31. Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10(6):239–247PubMedCrossRefGoogle Scholar
  32. Orman BA, Schumann RA Jr (1991) Comparison of near-infrared spectroscopy calibration methods for the prediction of protein, oil, and starch in maize grain. J Agric Food Chem 39(5):883–886CrossRefGoogle Scholar
  33. Peng XJ, Zhao Y, Li XM, Wu M, Chai WB, Sheng L, Wang Y, Dong Q, Jiang HY, Cheng BJ (2015) Genomewide identification, classification and analysis of NAC type gene family in maize. J Genet 94(3):377–390.  https://doi.org/10.1007/s12041-015-0526-9 PubMedCrossRefGoogle Scholar
  34. Peymanpour G, Marcone M, Ragaee S, Tetlow I, Lane CC, Seetharaman K, Bertoft E (2016) On the molecular structure of the amylopectin fraction isolated from “high-amylose” ae maize starches. Int J Biol Macromol 91:768–777PubMedCrossRefGoogle Scholar
  35. Qi X, Li S, Zhu Y, Zhao Q, Zhu D, Yu J (2017) ZmDof3, a maize endosperm-specific Dof protein gene, regulates starch accumulation and aleurone development in maize endosperm. Plant Mol Biol 93(1–2):7–20PubMedCrossRefGoogle Scholar
  36. Sablowski RW, Meyerowitz EM (1998) A homolog of no apical meristem is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92(1):93–103PubMedCrossRefGoogle Scholar
  37. Sekhon RS, Briskine R, Hirsch CN, Myers CL, Springer NM, Buell CR, Leon ND, Kaeppler SM (2013) Maize gene atlas developed by RNA sequencing and comparative evaluation of transcriptomes based on RNA sequencing and microarrays. PLoS One 8(4):e61005PubMedPubMedCentralCrossRefGoogle Scholar
  38. Syahariza Z, Sar S, Hasjim J, Tizzotti MJ, Gilbert RG (2013) The importance of amylose and amylopectin fine structures for starch digestibility in cooked rice grains. Food Chem 136(2):742–749PubMedCrossRefGoogle Scholar
  39. Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genom 284(3):173–183CrossRefGoogle Scholar
  40. Tester RF, Karkalas J, Qi X (2004) Starch—composition, fine structure and architecture. J Cereal Sci 39(2):151–165.  https://doi.org/10.1016/j.jcs.2003.12.001 CrossRefGoogle Scholar
  41. Tian Z, Qian Q, Liu Q, Yan M, Liu X, Yan C, Liu G, Gao Z, Tang S, Zeng D (2009) Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities. Proc Natl Acad Sci 106(51):21760–21765PubMedCrossRefGoogle Scholar
  42. Tran LSP, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16(9):2481–2498.  https://doi.org/10.1105/tpc.104.022699 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Wang TL, Bogracheva TY, Hedley CL (1998) Starch: as simple as A, B, C? J Exp Bot 49(320):481–502Google Scholar
  44. Wang JC, Xu H, Zhu Y, Liu QQ, Cai XL (2013) OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm. J Exp Bot 64(11):3453–3466PubMedPubMedCentralCrossRefGoogle Scholar
  45. Wang QQ, Liu JY, Wang Y, Zhao Y, Jiang HY, Cheng BJ (2015) Systematic analysis of the maize PHD-finger gene family reveals a subfamily involved in abiotic stress response. Int J Mol Sci 16(10):23517–23544PubMedPubMedCentralCrossRefGoogle Scholar
  46. Yan HB, Pan XX, Jiang HW, Wu GJ (2009) Comparison of the starch synthesis genes between maize and rice: copies, chromosome location and expression divergence. Theor Appl Genet 119(5):815–825PubMedCrossRefGoogle Scholar
  47. Zhang JJ, Chen J, Yi Q, Hu YF, Liu HM, Liu YH, Huang YB (2014) Novel role of ZmaNAC36 in co-expression of starch synthetic genes in maize endosperm. Plant Mol Biol 84(3):359–369.  https://doi.org/10.1007/s11103-013-0153-x PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life SciencesAnhui Agricultural UniversityHefeiPeople’s Republic of China
  2. 2.Institute of Horticulture of Anhui Academy of Agricultural SciencesHefeiPeople’s Republic of China

Personalised recommendations