Transcriptomic analysis reveals key factors in fruit ripening and rubbery texture caused by 1-MCP in papaya

BMC Plant Biol. 2019 Jul 12;19(1):309. doi: 10.1186/s12870-019-1904-x.

Abstract

Background: Ethylene promotes fruit ripening whereas 1-methylcyclopropene (1-MCP), a non-toxic antagonist of ethylene, delays fruit ripening via the inhibition of ethylene receptor. However, unsuitable 1-MCP treatment can cause fruit ripening disorders.

Results: In this study, we show that short-term 1-MCP treatment (400 nL•L- 1, 2 h) significantly delays papaya fruit ripening with normal ripening characteristics. However, long-term 1-MCP treatment (400 nL•L- 1, 16 h) causes a "rubbery" texture of fruit. The comparative transcriptome analysis showed that a total of 5529 genes were differently expressed during fruit ripening compared to freshly harvested fruits. Comprehensive functional enrichment analysis showed that the metabolic pathways of carbon metabolism, plant hormone signal transduction, biosynthesis of amino acids, and starch and sucrose metabolism are involved in fruit ripening. 1-MCP treatment significantly affected fruit transcript levels. A total of 3595 and 5998 differently expressed genes (DEGs) were identified between short-term 1-MCP, long-term 1-MCP treatment and the control, respectively. DEGs are mostly enriched in the similar pathway involved in fruit ripening. A large number of DEGs were also identified between long-term and short-term 1-MCP treatment, with most of the DEGs being enriched in carbon metabolism, starch and sucrose metabolism, plant hormone signal transduction, and biosynthesis of amino acids. The 1-MCP treatments accelerated the lignin accumulation and delayed cellulose degradation during fruit ripening. Considering the rubbery phenotype, we inferred that the cell wall metabolism and hormone signal pathways are closely related to papaya fruit ripening disorder. The RNA-Seq output was confirmed using RT-qPCR by 28 selected genes that were involved in cell wall metabolism and hormone signal pathways.

Conclusions: These results showed that long-term 1-MCP treatment severely inhibited ethylene signaling and the cell wall metabolism pathways, which may result in the failure of cell wall degradation and fruit softening. Our results reveal multiple ripening-associated events during papaya fruit ripening and provide a foundation for understanding the molecular mechanisms underlying 1-MCP treatment on fruit ripening and the regulatory networks.

Keywords: 1-MCP; Cell wall; Cellulose and lignin; Differentially expressed genes; Ethylene; Papaya; Rubbery texture; Transcriptome.

MeSH terms

  • Carica / genetics*
  • Carica / growth & development
  • Cyclopropanes / pharmacology*
  • Ethylenes / antagonists & inhibitors*
  • Fruit / genetics
  • Fruit / growth & development
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant
  • Plant Growth Regulators / antagonists & inhibitors*
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • Transcriptome*

Substances

  • Cyclopropanes
  • Ethylenes
  • Plant Growth Regulators
  • Plant Proteins
  • ethylene
  • 1-methylcyclopropene