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NAC transcription factors play an important role in ethylene biosynthesis, reception and signaling of tomato fruit ripening

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Abstract

NAC proteins comprise a large family of transcription factors that play important roles in diverse physiological processes during development. To explore the role of NAC transcription factors in the ripening of fruits, we predicted the secondary and tertiary structure as well as regulative function of the SNAC4 (SlNAC48, Accession number: NM 001279348.2) and SNAC9 (SlNAC19, Accession number: XM 004236996.2) transcription factors in tomato. We found that the tertiary structure of SNAC9 was similar to that of ATNAP, which played an important role in the fruit senescence and was required for ethylene stimulation. Likewise, the bio-function prediction results indicated that SNAC4 and SNAC9 participated in various plant hormone signaling and senescence processes. More information about SNACs was obtained by the application of VIGS (virus-induced gene silencing). The silencing of SNAC4 and SNAC9 dramatically repressed the LeACS2, LeACS4 and LeACO1 expression, which consequently led to the inhibition of the ripening process. The silencing of SNACs down-regulated the mRNA levels of the ethylene perception genes and, at the same time, suppressed the expression of ethylene signaling-related genes except for LeERF2 which was induced by the silencing of SNAC4. The expressions of LeRIN were different in two silenced fruits. In addition, the silencing of SNAC4 reduced its mRNA level, while the silencing of SNAC9 induced its expression. Furthermore, the silencing of LeACS4, LeACO1 and LeERF2 reduced the expression of SNAC4 and SNAC9, while the silencing of NR induced the expression of all of them. In particular, these results indicate that SNAC transcription factors bind to the promoter of the ethylene synthesis genes in vitro. This experimental evidence demonstrates that SNAC4 and SNAC9 could positively regulate the tomato fruit ripening process by functioning upstream of ethylene synthesis genes. These outcomes will be helpful to provide a theoretical foundation for further exploring the tomato fruit ripening and senescence mechanism.

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Acknowledgments

We are very grateful to Daqi Fu (China Agricultural University) for help in VIGS technology and experiment materials (Micro-Tom seeds and GV3101 agrobacterium strains). This work was supported by the National Natural Science Foundation of China (Grant No. 31171769; Grant No. 31470091; Grant No. 31201245).

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    1. School of Chemical Engineering and Technology, Tianjin University, Weijin Road, Tianjin, 300072, People’s Republic of China

      Xiaohong Kou, Chen Liu, Lihua Han, Shuang Wang & Zhaohui Xue

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    1. Xiaohong Kou
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    Correspondence to Xiaohong Kou or Zhaohui Xue.

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    This study was funded by the National Natural Science Foundation of China (Grant No. 31171769; Grant No. 31470091; Grant No. 31201245).

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    Xiaohong Kou declares that she has no conflict of interest. Chen Liu declares that she has no conflict of interest. Lihua Han declares that she has no conflict of interest. Shuang Wang declares that she has no conflict of interest. Zhaohui Xue declares that he has no conflict of interest.

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    This article does not contain any studies with human participants or animals performed by any of the authors.

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    Communicated by C. Gebhardt.

    X. Kou and C. Liu contributed equally to this paper.

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    Kou, X., Liu, C., Han, L. et al. NAC transcription factors play an important role in ethylene biosynthesis, reception and signaling of tomato fruit ripening. Mol Genet Genomics 291, 1205–1217 (2016). https://doi.org/10.1007/s00438-016-1177-0

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