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. 2019 Mar 1:6:36.
doi: 10.1038/s41438-019-0117-7. eCollection 2019.

EGTA reduces the inflorescence stem mechanical strength of herbaceous peony by modifying secondary wall biosynthesis

Yuhan Tang #  1 , Daqiu Zhao #  1 , Jiasong Meng  1 , Jun Tao  1
Affiliations

EGTA reduces the inflorescence stem mechanical strength of herbaceous peony by modifying secondary wall biosynthesis

Yuhan Tang et al. Hortic Res. .

Abstract

The mechanical strength of inflorescence stems is an important trait in cut flowers. Calcium ions (Ca2+) play a pivotal role in maintaining stem strength, but little is known about the underlying molecular mechanisms. In this study, we treated herbaceous peony (Paeonia lactiflora Pall.) with ethyl glycol tetraacetic acid (EGTA), an effective Ca2+ chelator, and used morphology indicators, spectroscopic analysis, histochemical staining, electron microscopy, and proteomic techniques to investigate the role of Ca2+ in inflorescence stem mechanical strength. The EGTA treatment reduced the mechanical strength of inflorescence stems, triggered the loss of Ca2+ from cell walls, and reduced lignin in thickened secondary walls in xylem cells as determined by spectroscopic analysis and histochemical staining. Electron microscopy showed that the EGTA treatment also resulted in significantly fewer xylem cell layers with thickened secondary walls as well as in reducing the thickness of these secondary walls. The proteomic analysis showed 1065 differentially expressed proteins (DEPs) at the full-flowering stage (S4). By overlapping the Kyoto encyclopedia of genes and genomes (KEGG) and gene ontology (GO) analysis results, we identified 43 DEPs involved in signal transduction, transport, energy metabolism, carbohydrate metabolism, and secondary metabolite biosynthesis. Using quantitative real-time polymerase chain reaction (qRT-PCR) analysis, we showed that EGTA treatment inhibited Ca2+ sensors and secondary wall biosynthesis-related genes. Our findings revealed that EGTA treatment reduced the inflorescence stem mechanical strength by reducing lignin deposition in xylem cells through altering the expression of genes involved in Ca2+ binding and secondary wall biosynthesis.

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Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1. Effects of EGTA treatment on morphological indices and photosynthetic characteristics of P. lactiflora at four developmental stages.
a Photographs of inflorescence stems. Bar = 5 cm. b Morphological indices and photosynthetic characteristics. The values represent the means ± SD, and different letters indicate significant differences (P < 0.05). Pn, photosynthesis rate; Gs, stomatal conductance; Tr, transpiration rate; S1, flower-bud stage; S2, pigmented stage; S3, unfold-petal stage; S4, full-flowering stage
Fig. 2
Fig. 2. Effects of EGTA treatment on cell wall compositions of P. lactiflora inflorescence stems.
a Absorption FTIR spectra of the cell wall in the 4000–400 cm-1 and 1800–800 cm-1 regions. b Transverse sections of 8 µm thickness were stained with phloroglucinol-HCl, which selectively stains lignified cell walls. Bars, 100μm. FTIR, Fourier-transform infrared spectroscopy; S1, flower-bud stage; S2, pigmented stage; S3, unfold-petal stage; S4, full-flowering stage
Fig. 3
Fig. 3. Effects of EGTA treatment on the microstructures of P. lactiflora inflorescence stems at S1 and S4.
a Scanning electron microscopy. Micrographs of partial enlargement of the regions are marked by the arrow. Bars, 100μm. b Optical microscope. Bars, 50μm. c Transmission electron microscopy. Bars, 10μm. Ep, epidermis; Co, cortex; Xy, xylem; Pi, pith; S1, flower bud stage; S4, full flowering stage
Fig. 4
Fig. 4. Effects of EGTA treatment on the proteome of P. lactiflora inflorescence stems.
a GO enrichment analysis of differentially expressed proteins related to mechanical strength-related processes. b Top 10 KEGG pathways and 10 KEGG enrichment analyses of differentially expressed proteins related to mechanical strength-related processes. *Differentially expressed proteins and significantly enriched pathways. DEPs, differentially expressed proteins; GO, gene ontology; KEGG, Kyoto encyclopedia of genes and genomes
Fig. 5
Fig. 5
The log2 relative expression levels of 43 overlapped differentially expressed proteins from KEGG and GO analysis. GO, gene ontology; KEGG, Kyoto encyclopedia of genes and genomes
Fig. 6
Fig. 6. Effects of EGTA treatment on key genes related to mechanical strength and a proposed pathway for EGTA-mediated reduction of mechanical strength of P. lactiflora inflorescence stems.
a Heat maps of the expression of 23 genes involved in Ca signal transduction and secondary cell wall biosynthesis at four developmental stages. PM, plasma membrane; SCW, secondary cell wall; PCW, primary cell wall; ML, middle lamella. b Proposed pathway for EGTA-mediated weakness of the mechanical strength of Paeonia lactiflora inflorescence stems. ML, middle lamella; PCW, primary cell wall; PM, plasma membrane; SCW, secondary cell wall; S1, flower-bud stage; S2, pigmented stage; S3, unfold-petal stage; S4, full-flowering stage
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