Production of reactive oxygen species by PuRBOHF is critical for stone cell development in pear fruit

Xiaoqian Wang , Siqi Liu , Huili Sun , Chunyan Liu , Xinyue Li , Yang Liu , Deguo Lyu , Guodong Du

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 249

PDF (2099KB)
Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :249 DOI: 10.1038/s41438-021-00674-0
Article
research-article
Production of reactive oxygen species by PuRBOHF is critical for stone cell development in pear fruit
Author information +
History +
PDF (2099KB)

Abstract

The production of reactive oxygen species (ROS) by NADPH oxidase, which is also referred to as respiratory burst oxidase homolog (RBOH), affects several processes in plants. However, the role of RBOHs in cell wall lignification is not well understood. In this study, we show that PuRBOHF, an RBOH isoform, plays an important role in secondary wall formation in pear stone cells. ROS were closely associated with lignin deposition and stone cell formation according to microscopy data. In addition, according to the results of an in situ hybridization analysis, the stage-specific expression of PuRBOHF was higher in stone cells than in cells of other flesh tissues. Inhibitors of RBOH activity suppressed ROS accumulation and stone cell lignification in pear fruit. Moreover, transient overexpression of PuRBOHF caused significant changes in the amount of ROS and lignin that accumulated in pear fruit and flesh calli. We further showed that PuMYB169 regulates PuRBOHF expression, while PuRBOHF-derived ROS induces the transcription of PuPOD2 and PuLAC2. The findings of this study indicate that PuRBOHF-mediated ROS production, which is regulated by a lignin-related transcriptional network, is essential for monolignol polymerization and stone cell formation in pear fruit.

Cite this article

Download citation ▾
Xiaoqian Wang, Siqi Liu, Huili Sun, Chunyan Liu, Xinyue Li, Yang Liu, Deguo Lyu, Guodong Du. Production of reactive oxygen species by PuRBOHF is critical for stone cell development in pear fruit. Horticulture Research, 2021, 8 (1) : 249 DOI:10.1038/s41438-021-00674-0

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Bassil, N. & Postman, J. D. Identification of European and Asian pears using EST-SSRs from Pyrus. Genet. Resour. Crop Ev 57, 357-370 (2010).

[2]

Liu, Q. et al. Genetic diversity and population structure of pear (Pyrus spp.) collections revealed by a set of core genome-wide SSR markers. Tree Genet. Genomes 11, 1-22 (2015).

[3]

Yan, C. et al. Stone cell distribution and lignin structure in various pear varieties. Sci. Hortic.-Amst. 174, 142-150 (2014).

[4]

Xue, C. et al. PbrMYB169 positively regulates lignification of stone cells in pear fruit. J. Exp. Bot. 70, 1801-1814 (2019).

[5]

Cai, Y. et al. Study of the structure and biosynthetic pathway of lignin in stone cells of pear. Sci. Hortic. 125, 374-379 (2010).

[6]

Li, S. H., Schneider, B. & Gershenzon, J. Microchemical analysis of laser-microdissected stone cells of Norway spruce by cryogenic nuclear magnetic resonance spectroscopy. Planta 225, 771-779 (2007).

[7]

Choi, J. & Lee, S. Distribution of stone cell in Asian, Chinese, and European pear fruit and its morphological changes. J. Appl Bot. Food Qual. 86, 185-189 (2013).

[8]

Shinya, T. et al. Transcriptional profiles of hybrid Eucalyptus genotypes with contrasting lignin content reveal that monolignol biosynthesis-related genes regulate wood composition. Front. Plant Sci. 7, 443 (2016).

[9]

Gong, X. et al. PbMC1a/1b regulates lignification during stone cell development in pear (Pyrus bretschneideri) fruit. Hortic. Res.-Engl. 7, 1-13 (2020).

[10]

Li, D. et al. Hydrogen peroxide accelerated the lignification process of bamboo shoots by activating the phenylpropanoid pathway and programmed cell death in postharvest storage. Postharvest Biol. Tec. 153, 79-86 (2019).

[11]

Yoon, J., Choi, H. & An, G. Roles of lignin biosynthesis and regulatory genes in plant development. J. Integr. Plant Biol. 57, 902-912 (2015).

[12]

Wang, Y., Chantreau, M., Sibout, R. & Hawkins, S. Plant cell wall lignification and monolignol metabolism. Front Plant Sci. 4, 220 (2013).

[13]

Barros, J., Serk, H., Granlund, I. & Pesquet, E. The cell biology of lignification in higher plants. Ann. Bot. 115, 1053-1074 (2015).

[14]

Chen, Q. & Yang, G. Signal function studies of ROS, especially RBOH-dependent ROS, in plant growth, development and environmental stress. J. Plant Growth Regul. 39, 157-171 (2020).

[15]

Orman-Ligeza, B. et al. RBOH-mediated ROS production facilitates lateral root emergence in Arabidopsis. Development 143, 3328-3339 (2016).

[16]

Sierla, M., Waszczak, C., Vahisalu, T. & Kangasjärvi, J. Reactive oxygen species in the regulation of stomatal movements. Plant Physiol. 171, 1569-1580 (2016).

[17]

Singh, R. et al. Reactive oxygen species (ROS): beneficial companions of plants’ developmental processes. Front Plant Sci. 7, 1299 (2016).

[18]

Xie, H. T., Wan, Z. Y., Li, S. & Zhang, Y. Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. Plant Cell 26, 2007-2023 (2014).

[19]

Yang, X. et al. The NADPH-oxidase LsRbohC1 plays a role in lettuce (Lactuca sativa) seed germination. Plant Physiol. Bioch. 154, 751-757 (2020).

[20]

Yamauchi, T. et al. An NADPH oxidase RBOH functions in rice roots during lysigenous aerenchyma formation under oxygen-deficient conditions. Plant Cell 29, 775-790 (2017).

[21]

Lee, Y., Rubio, M. C., Alassimone, J. & Geldner, N. A mechanism for localized lignin deposition in the endodermis. Cell 153, 402-412 (2013).

[22]

Liu, Q. et al. Transcriptional and physiological analyses identify a regulatory role for hydrogen peroxide in the lignin biosynthesis of copper-stressed rice roots. Plant Soil 387, 323-336 (2015).

[23]

Heng, W. et al. Relationship between H2O2 in polyamine metabolism and lignin in the exocarp of a russet mutant of ‘Dangshansuli’ pear (Pyrus bretschneideri Rehd.) . Plant Mol. Biol. Rep. 34, 1056-1063 (2016).

[24]

Liu, Y. & He, C. Regulation of plant reactive oxygen species (ROS) in stress responses: learning from AtRBOHD. Plant Cell Rep. 35, 995-1007 (2016).

[25]

Lee, D. et al. Regulation of reactive oxygen species during plant immunity through phosphorylation and ubiquitination of RBOHD. Nat. Commun. 11, 1-16 (2020).

[26]

Müller, K., Carstens, A. C., Linkies, A., Torres, M. A. & Leubner‐Metzger, G. The NADPH-oxidase AtrbohB plays a role in Arabidopsis seed after‐ripening. N. Phytol. 184, 885-897 (2009).

[27]

Foreman, J. et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442-446 (2003).

[28]

Cheng, X. et al. In silico genome-wide analysis of respiratory burst oxidase homolog (RBOH) family genes in five fruit-producing trees, and potential functional analysis on lignification of stone cells in chinese white pear. Cells 8, 520 (2019).

[29]

Zhang, J. et al. Comparison of the transcriptomic analysis between two Chinese white pear (Pyrus bretschneideri Rehd.) genotypes of different stone cells contents. PLoS ONE 12, e0187114 (2017).

[30]

Anderson, N. A. et al. Manipulation of guaiacyl and syringyl monomer biosynthesis in an Arabidopsis cinnamyl alcohol dehydrogenase mutant results in atypical lignin biosynthesis and modified cell wall structure. Plant Cell 27, 2195-2209 (2015).

[31]

Tao, S., Khanizadeh, S., Zhang, H. & Zhang, S. Anatomy, ultrastructure and lignin distribution of stone cells in two Pyrus species. Plant Sci. 176, 413-419 (2009).

[32]

Brennan, T. & Frenkel, C. Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol. 59, 411-416 (1977).

[33]

Choi, H. W., Kim, Y. J., Lee, S. C., Hong, J. K. & Hwang, B. K. Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens . Plant Physiol. 145, 890-904 (2007).

[34]

Chen, Z. et al. The AtrbohF-dependent regulation of ROS signaling is required for melatonin-induced salinity tolerance in Arabidopsis. Free Radic. Bio Med. 108, 465-477 (2017).

[35]

Bestwick, C. S., Brown, I. R., Bennett, M. H. & Mansfield, J. W. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9, 209-221 (1997).

[36]

Zhang, J. et al. Reactive oxygen species produced via plasma membrane NADPH oxidase regulate anthocyanin synthesis in apple peel. Planta 240, 1023-1035 (2014).

[37]

Sagi, M. & Fluhr, R. Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol. 126, 1281-1290 (2001).

[38]

Cheng, X. et al. 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, 1602-1613 (2017).

[39]

Xue, C. et al. PbrmiR397a regulates lignification during stone cell development in pear fruit. Plant Biotechnol. J. 17, 103-117 (2019a).

[40]

Bai, S. et al. BBX16, a B-box protein, positively regulates light-induced anthocyanin accumulation by activating MYB10 in red pear. Plant Biotechnol. J. 17, 1985-1997 (2019).

[41]

Wu, A. et al. JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell. 24, 482-506 (2012).

[42]

He, J. et al. DEXH Box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. Plant Cell. 24, 1815-1833 (2012).

[43]

Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907 (1987).

[44]

Yang, C. et al. Activation of ethylene signaling pathways enhances disease resistance by regulating ROS and phytoalexin production in rice. Plant J. 89, 338-353 (2017).

[45]

Torres, M. A. & Dangl, J. L. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol. 8, 397-403 (2005).

[46]

Cepauskas, D. et al. Characterization of apple NADPH oxidase genes and their expression associated with oxidative stress in shoot culture in vitro. Plant Cell, Tiss. Org. 124, 621-633 (2016).

[47]

Wang, X. et al. Biochemical characterization and expression analysis of lignification in two pear (Pyrus ussuriensis Maxim.) varieties with contrasting stone cell content. Protoplasma 257, 261-274 (2020).

[48]

Gayomba, S. R. & Muday, G. K. Flavonols regulate root hair development by modulating accumulation of reactive oxygen species in the root epidermis. Development 147, dev185819 (2020).

[49]

Denness, L. et al. Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species-and jasmonic acid-dependent process in Arabidopsis. Plant Physiol. 156, 1364-1374 (2011).

[50]

Lee, Y. et al. A lignin molecular brace controls precision processing of cell walls critical for surface integrity in Arabidopsis. Cell 173, 1468-1480 (2018).

[51]

Kärkönen, A. & Kuchitsu, K. Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112, 22-32 (2015).

[52]

Barceló, A. R. Xylem parenchyma cells deliver the H2O2 necessary for lignification in differentiating xylem vessels . Planta 220, 747-756 (2005).

PDF (2099KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/