Abstract
Main Conclusion
For the first time, stone cells in pear and apple pedicel were studied. The lignification of the pedicel outer part was correlated with flesh, and the secondary cell wall biosynthesis genes were activated.
Abstract
Fruit pedicels act as bridges between the fruit and the shoot. They have secondary thickened cell walls that presumably function in mechanical support, water and nutrient transport. Stone cells are cells with a secondary cell wall thickening. In pears, yet not in apples, the stone cells affect the flesh texture. There have been few reports on stone cell formation in pear and apple pedicels; therefore, we studied these cells for the first time. The apple pedicel had few stone cells in the cortex. The formation of stone cells in pear continued until seven weeks after flowering (WAF), and the density was significantly higher than in apple. The stone cell formation degree (SFD) of pear was 3.6–7.1 times higher than that of apple. Total lignin and lignin non-condensed structure (G and S units) content in the pear pedicle outer part was 1.5–2.7 times higher than that of the apple at harvest. The SFD of the pedicel outer part had a positive correlation with the G and S units content of the flesh. The total lignin and G and S units content between flesh and the pedicel outer part were positively correlated. Correlation analysis revealed a positive relationship between fruit and pedicel formation of the stone cells. The WGCNA showed that NST3 was linked to NAC028, MYB46, CESA, POD, LAC, and VSR6. These genes were highly expressed in the outer part of the pear pedicel, while they were suppressed in that issue of the apple at 4 WAF.






Data and material availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- ARF:
-
Auxin response factor
- CESA:
-
Cellulose synthase A catalytic subunit
- G-lignin:
-
Guaiacyl lignin
- LAC:
-
Laccase
- NST:
-
NAC secondary wall thickening promoting factor
- PLD:
-
Pedicel lignification degree
- S-lignin:
-
Syringyl lignin
- SFD:
-
Stone cell formation degree
- TF:
-
Transcription factor
- WAF:
-
Weeks after flowering
References
Bao W, O’Malley DM, Whetten R, Sederoff RR (1993) A laccase associated with lignification in loblolly pine xylem. Science 260(5108):672–674
Barros J, Serk H, Granlund I, Pesquet E (2015) The cell biology of lignification in higher plants. Ann Bot 115(7):1053–1074
Berthet S, Demont-Caulet N, Pollet B, Bidzinski P, Cezard L, Le Bris P, Borrega N, Herve J, Blondet E, Balzergue S, Lapierre C, Jouanin L (2011) Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. Plant Cell 23(3):1124–1137
Cai Y, Li G, Nie J, Lin Y, Nie F, Zhang J, Xu Y (2010) Study of the structure and biosynthetic pathway of lignin in stone cells of pear. Sci Hortic 125(3):374–379
Cao Y, Han Y, Li D, Lin Y, Cai Y (2016) Systematic analysis of the 4-coumarate: coenzyme A ligase (4CL) related genes and expression profiling during fruit development in the Chinese pear. Genes (Basel) 7(10):89
Chagne D, Crowhurst RN, Pindo M, Thrimawithana A, Deng C et al (2014) The draft genome sequence of European pear (Pyrus communis L. ‘Bartlett’). PLoS One 9(4):e92644
Cheng X, Xiong Y, Li DH, Cheng J, Cao YP, Yan CC, Jin Q, Sun N, Cai YP, Lin Y (2016) Bioinformatic and expression analysis of the OMT gene family in Pyrus bretschneideri cv. Dangshan Su. Genet Mol Res. https://doi.org/10.4238/gmr.15038664
Cheng X, Li M, Li D, Zhang J, Jin Q, Sheng L, Cai Y, Lin Y (2017a) Characterization and analysis of CCR and CAD gene families at the whole-genome level for lignin synthesis of stone cells in pear (Pyrus bretschneideri) fruit. Biol Open 6(11):1602–1613
Cheng X, Yan C, Zhang J, Ma C, Li S, Jin Q, Zhang N, Cao Y, Lin Y, Cai Y (2017b) The effect of different pollination on the expression of Dangshan Su pear microRNA. Biomed Res Int 2017:2794040
Cheng X, Li G, Ma C, Abdullah M, Zhang J, Zhao H, Jin Q, Cai Y, Lin Y (2019) Comprehensive genome-wide analysis of the pear (Pyrus bretschneideri) laccase gene (PbLAC) family and functional identification of PbLAC1 involved in lignin biosynthesis. PLoS One 14(2):e0210892
Cheng X, Zhang J, Wang H, Chen T, Li G, Yan C, Jin Q, Lin Y, Cai Y (2020) Effects of metaxenia on stone cell formation in pear (Pyrus bretschneideri) based on transcriptomic analysis and functional characterization of the lignin-related gene PbC4H2. Forests 11(1):53
Cui Z, Sun H, Lu Y, Ren L, Xu X, Li D, Wang R, Ma C (2022) Variations in pedicel structural properties among four pear species (Pyrus): Insights into the relationship between the fruit characteristics and the pedicel structure. Front Plant Sci 13:815283
Daccord N, Celton JM, Linsmith G, Becker C, Choisne N, Schijlen E, van de Geest H et al (2017) High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet 49(7):1099–1106
Dardick C, Callahan AM (2014) Evolution of the fruit endocarp: Molecular mechanisms underlying adaptations in seed protection and dispersal strategies. Front Plant Sci 5:284
Dong X, Wang Z, Tian L, Zhang Y, Qi D, Huo H, Xu J, Li Z, Liao R, Shi M, Wahocho SA, Liu C, Zhang S, Tian Z, Cao Y (2019) De novo assembly of a wild pear (Pyrus betuleafolia) genome. Plant Biotechnol J 18(2):581–595
Drazeta L, Lang A, Cappellini C, Hall AJ, Volz RK, Jameson PE (2004) Vessel differentiation in the pedicel of apple and the effects of auxin transport inhibition. Physiol Plant 120(1):162–170
Folta KM, Gardiner SE (2009) Genetics and genomics of Rosaceae. Springer, New York
Herremans E, Verboven P, Hertog ML, Cantre D, van Dael M, De Schryver T, Van Hoorebeke L, Nicolai BM (2015) Spatial development of transport structures in apple (Malus x domestica Borkh.) fruit. Front Plant Sci 6:679
Horbens M, Feldner A, Hofer M, Neinhuis C (2014) Ontogenetic tissue modification in Malus fruit peduncles: The role of sclereids. Ann Bot 113(1):105–118
Itoyama H, Nakagawa ACS, Ariyoshi Y, Ario N, Yuasa T, Iwaya-Inoue M, Ishibashi Y (2020) Lignin deposits in pedicel xylem vessels regulate water transport during seed maturation in soybean. Crop Sci 60(2):954–960
Kasirajan L, Hoang NV, Furtado A, Botha FC, Henry RJ (2018) Transcriptome analysis highlights key differentially expressed genes involved in cellulose and lignin biosynthesis of sugarcane genotypes varying in fiber content. Sci Rep 8(1):11612
Katahira R, Nakatsubo F (2001) Determination of nitrobenzene oxidation products by GC and 1H-NMR spectroscopy using 5-iodovanillin as a new internal standard. J Wood Sci 47:378–382
Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinform 9:559
Li M, Cheng C, Zhang X, Zhou S, Wang C, Ma C, Yang S (2019) PpNAC187 enhances lignin synthesis in ‘Whangkeumbae’ Pear (Pyrus pyrifolia) ‘Hard-End’ fruit. Molecules 24(23):4338
Lin SY, Dence CW (eds) (1992) Methods in lignin chemistry. Springer Series in Wood Science, Springer, Berlin, Heidelberg
Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19(1):270–280
Qu G, Peng D, Yu Z, Chen X, Cheng X, Yang Y, Ye T, Lv Q, Ji W, Deng X, Zhou B (2021) Advances in the role of auxin for transcriptional regulation of lignin biosynthesis. Fun Plant Biol 48(8):743–754
Sakamoto S, Mitsuda N (2015) Reconstitution of a secondary cell wall in a secondary cell wall-deficient Arabidopsis mutant. Plant Cell Physiol 56(2):299–310
Shirasawa K, Itai A, Isobe S (2021) Chromosome-scale genome assembly of Japanese pear (Pyrus pyrifolia) variety ‘Nijisseiki.’ DNA Res. https://doi.org/10.1093/dnares/dsab001
Smith WW (1935) The course of stone cell formation in pear fruits. Plant Physiol 10(4):587–611
Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A et al (2010) The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet 42(10):833–839
Wang R, Xue Y, Fan J, Yao JL, Qin M, Lin T, Lian Q, Zhang M, Li X, Li J, Sun M, Song B, Zhang J, Zhao K, Chen X, Hu H, Fei Z, Xue C, Wu J (2021) A systems genetics approach reveals PbrNSC as a regulator of lignin and cellulose biosynthesis in stone cells of pear fruit. Genome Biol 22(1):313
Wu J, Zhang SL, Li XL (2019) The genome of pear. In: Korban SS (ed) The pear genome. Springer, Cham, pp 133–143
Xu Q, Wang W, Zeng J, Zhang J, Grierson D, Li X, Yin X, Chen K (2015) A NAC transcription factor, EjNAC1, affects lignification of loquat fruit by regulating lignin. Postharvest Biol Technol 102:25–31
Xu XF, Wang B, Feng YF, Xue JS, Qian XX, Liu SQ, Zhou J, Yu YH, Yang NY, Xu P, Yang ZN (2019) Auxin response factor17 directly regulates MYB108 for anther dehiscence. Plant Physiol 181(2):645–655
Xue H, Wang S, Yao JL, Deng CH, Wang L, Su Y, Zhang H, Zhou H, Sun M, Li X, Yang J (2018) Chromosome level high-density integrated genetic maps improve the Pyrus bretschneideri ‘DangshanSuli’ v1.0 genome. BMC Genom 19(1):833
Yan C, Yin M, Zhang N, Jin Q, Fang Z, Lin Y, Cai Y (2014) Stone cell distribution and lignin structure in various pear varieties. Sci Hortic 174:142–150
Zhang C, Tanabe K, Tamura F, Itai A, Yoshida M (2007a) Roles of gibberellins in increasing sink demand in Japanese pear fruit during rapid fruit growth. Plant Growth Regul 52(2):161–172
Zhang C, Tanabe K, Tani H, Nakajima H, Mori M, Sakuno E (2007b) Biologically active gibberellins and abscisic acid in fruit of two late-maturing Japanese pear cultivars with contrasting fruit size. J Am Soc Hortic Sci 132(4):452–458
Zhang MY, Xue C, Xu L, Sun H, Qin MF, Zhang S, Wu J (2016) Distinct transcriptome profiles reveal gene expression patterns during fruit development and maturation in five main cultivated species of pear (Pyrus L.). Sci Rep 6(28130):28130
Zhang L, Hu J, Han X, Li J, Gao Y, Richards CM, Zhang C, Tian Y, Liu G, Gul H, Wang D, Tian Y, Yang C, Meng M, Yuan G, Kang G, Wu Y, Wang K, Zhang H, Wang D, Cong P (2019) A high-quality apple genome assembly reveals the association of a retrotransposon and red fruit colour. Nat Commun 10(1):1494
Zhang L, Kamitakahara H, Murayama H, Ohsako T, Itai A (2020) Analysis of fruit lignin content, composition, and linkage types in pear cultivars and related species. J Agric Food Chem 68(8):2493–2505
Zhao Q, Nakashima J, Chen F, Yin Y, Fu C, Yun J, Shao H, Wang X, Wang ZY, Dixon RA (2013) LACCASE is necessary and nonredundant with PEROXIDASE for lignin polymerization during vascular development in Arabidopsis. Plant Cell 25(10):3976–3987
Acknowledgements
This work was supported in part by grants-in-aid from the Japanese Society for the Promotion of Science (no.16H04874 and no. 20H02979). We would like to thank Editage (http://www.editage.com) for English language editing.
Author information
Authors and Affiliations
Contributions
L.Z. performed the experiments. H.K. and T.T. provided facilities for lignin analysis. L.Z., S.S., N.M., and A.I. analyzed the data. L.Z. and A.I. wrote the manuscript. A.I. conceived the experiments. A.I. and L.Z. designed the experiments. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interests.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, L., Kamitakahara, H., Takano, T. et al. Stone cell formation in the pedicel of pears and apples. Planta 258, 85 (2023). https://doi.org/10.1007/s00425-023-04240-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04240-x