Glycine-rich RNA-binding cofactor RZ1AL is associated with tomato ripening and development

Xindi Li , Yongfang Yang , Ni Zeng , Guiqin Qu , Daqi Fu , Benzhong Zhu , Yunbo Luo , Oren Ostersetzer-Biran , Hongliang Zhu

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhac134

PDF (1416KB)
Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhac134 DOI: 10.1093/hr/uhac134
Article
research-article
Glycine-rich RNA-binding cofactor RZ1AL is associated with tomato ripening and development
Author information +
History +
PDF (1416KB)

Abstract

Tomato ripening is a complex and dynamic process coordinated by many regulatory elements, including plant hormones, transcription factors, and numerous ripening-related RNAs and proteins. Although recent studies have shown that some RNA-binding proteins are involved in the regulation of the ripening process, understanding of how RNA-binding proteins affect fruit ripening is still limited. Here, we report the analysis of a glycine-rich RNA-binding protein, RZ1A-Like (RZ1AL), which plays an important role in tomato ripening, especially fruit coloring. To analyze the functions of RZ1AL in fruit development and ripening, we generated knockout cr-rz1al mutant lines via the CRISPR/Cas9 gene-editing system. Knockout of RZ1AL reduced fruit lycopene content and weight in the cr-rz1al mutant plants. RZ1AL encodes a nucleus-localized protein that is associated with Cajal-related bodies. RNA-seq data demonstrated that the expression levels of genes that encode several key enzymes associated with carotenoid biosynthesis and metabolism were notably downregulated in cr-rz1al fruits. Proteomic analysis revealed that the levels of various ribosomal subunit proteins were reduced. This could affect the translation of ripening-related proteins such as ZDS. Collectively, our findings demonstrate that RZ1AL may participate in the regulation of carotenoid biosynthesis and metabolism and affect tomato development and fruit ripening.

Cite this article

Download citation ▾
Xindi Li, Yongfang Yang, Ni Zeng, Guiqin Qu, Daqi Fu, Benzhong Zhu, Yunbo Luo, Oren Ostersetzer-Biran, Hongliang Zhu. Glycine-rich RNA-binding cofactor RZ1AL is associated with tomato ripening and development. Horticulture Research, 2022, 9 (1) : uhac134 DOI:10.1093/hr/uhac134

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Wang RF, Angenent GC, Seymour G et al. Revisiting the role of master regulators in tomato ripening. Trends Plant Sci. 2020; 25: 291-301.

[2]

Klee HJ, Giovannoni JJ . Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet. 2011; 45: 41-59.

[3]

Giovannoni J, Nguyen C, Ampofo B et al. The epigenome and transcriptional dynamics of fruit ripening. Annu Rev Plant Biol. 2017; 68: 61-84.

[4]

Xiong C, Luo D, Lin A et al. A tomato B-box protein SlBBX20 modulates carotenoid biosynthesis by directly activating PHYTOENE SYNTHASE 1, and is targeted for 26S proteasome-mediated degradation. New Phytol. 2019; 221: 279-94.

[5]

Wang PW, Wang Y, Wang W et al. Ubiquitination of phytoene synthase 1 precursor modulates carotenoid biosynthesis in tomato. Commun Biol 2020; 3: 730.

[6]

Li XD, Wang Y, Chen S et al. Lycopene is enriched in tomato fruit by CRISPR/Cas9-mediated multiplex genome editing. Front Plant Sci 2018; 9: 559.

[7]

Karniel U, Koch A, Zamir D et al. Development of zeaxanthin-rich tomato fruit through genetic manipulations of carotenoid biosynthesis. Plant Biotechnol J. 2020; 18: 2292-303.

[8]

Yang YF, Liu X, Wang K et al. Molecular and functional diversity of organelle RNA editing mediated by RNA recognition motif-containing protein ORRM4 in tomato. New Phytol. 2020; 228: 570-85.

[9]

Li S, Zhu B, Pirrello J et al. Roles of RIN and ethylene in tomato fruit ripening and ripening-associated traits. New Phytol. 2020; 226: 460-75.

[10]

Xiao Y, Kang B, Li M et al. Transcription of lncRNA ACoS-AS1 is essential to trans-splicing between SlPsy1 and ACoS-AS1 that causes yellow fruit in tomato. RNA Biol. 2020; 17: 596-607.

[11]

Kalinina NO, Makarova S, Makhotenko A et al. The multiple functions of the nucleolus in plant development, disease and stress responses. Front Plant Sci 2018; 9: 132.

[12]

Muller-McNicoll M, Neugebauer KM . How cells get the message: dynamic assembly and function of mRNA-protein complexes. Nat Rev Genet. 2013; 14: 275-87.

[13]

Younis I, Dittmar K, Wang W et al. Minor introns are embedded molecular switches regulated by highly unstable U6atac snRNA. eLife. 2013; 2: e00780.

[14]

Gerstberger S, Hafner M, Tuschl T . A census of human RNA-binding proteins. Nat Rev Genet. 2014; 15: 829-45.

[15]

Jangi M, Sharp PA . Building robust transcriptomes with master splicing factors. Cell. 2014; 159: 487-98.

[16]

Vandivier LE, Anderson SJ, Foley SW et al. The conservation and function of RNA secondary structure in plants. Annu Rev Plant Biol. 2016; 67: 463-88.

[17]

Zuo Y, Feng F, Qi WW et al. Dek42 encodes an RNA-binding protein that affects alternative pre-mRNA splicing and maize kernel development. J Integr Plant Biol. 2019; 61: 728-48.

[18]

Lorkovic ZJ, Barta A . Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res. 2002; 30: 623-35.

[19]

Varani G, Nagai K . RNA recognition by RNP proteins during RNA processing. Annu Rev Biophys Biomol Struct. 1998; 27: 407-45.

[20]

Staiger D, Zecca L, Kirk DAW et al. The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA. Plant J. 2003; 33: 361-71.

[21]

Wippel HH, Malgarin JS, Inoue AH et al. Unveiling the partners of the DRBD2-mRNP complex, an RBP in Trypanosoma cruzi and ortholog to the yeast SR-protein Gbp2. BMC Microbiol. 2019; 19: 128.

[22]

Fusaro AF, Sachetto-Martins G . Blooming time for plant glycine-rich proteins. Plant Signal Behav. 2007; 2: 386-7.

[23]

Ortega-Amaro MA, Rodriguez-Hernandez AA, Rodriguez-Kessler M et al. Overexpression of AtGRDP2, a novel glycine-rich domain protein, accelerates plant growth and improves stress tolerance. Front Plant Sci. 2015; 5: 782.

[24]

Silverman IM, Li F, Gregory BD . Genomic era analyses of RNA secondary structure and RNA-binding proteins reveal their significance to post-transcriptional regulation in plants. Plant Sci. 2013; 205-206: 55-62.

[25]

Heintzen C, Melzer S, Fischer R et al. A light-entrained and temperature-entrained circadian clock controls expression of transcripts encoding nuclear proteins with homology to RNA-binding proteins in meristematic tissue. Plant J. 1994; 5: 799-813.

[26]

Mangeon A, Junqueira RM, Sachetto-Martins G . Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal Behav 2010; 5: 99-104.

[27]

Czolpinska M, Rurek M . Plant glycine-rich proteins in stress response: an emerging, still prospective story. Front Plant Sci 2018; 9: 302.

[28]

Xu T, Gu L, Choi MJ et al. Comparative functional analysis of wheat (Triticum aestivum) zinc finger-containing glycine-rich RNA-binding proteins in response to abiotic stresses. PLoS One. 2014; 9: e96877.

[29]

Kim YO, Pan S, Jung CH et al. A zinc finger-containing glycine-rich RNA-binding protein, atRZ-1a, has a negative impact on seed germination and seedling growth of Arabidopsis thaliana under salt or drought stress conditions. Plant Cell Physiol. 2007; 48: 1170-81.

[30]

Xu T, Han JH, Kang H . Structural features important for the RNA chaperone activity of zinc finger-containing glycine-rich RNA-binding proteins from wheat (Triticum aestivum) and rice (Oryza sativa). Phytochemistry. 2013; 94: 28-35.

[31]

Park YR, Choi MJ, Park SJ et al. Three zinc-finger RNA-binding proteins in cabbage (Brassica rapa) play diverse roles in seed germination and plant growth under normal and abiotic stress conditions. Physiol Plant. 2017; 159: 93-106.

[32]

Kim WY, Kim JY, Jung HJ et al. Comparative analysis of Arabidopsis zinc finger-containing glycine-rich RNA-binding proteins during cold adaptation. Plant Physiol Biochem. 2010; 48: 866-72.

[33]

Kim YO, Kim JS, Kang H . Cold-inducible zinc finger-containing glycine-rich RNA-binding protein contributes to the enhancement of freezing tolerance in Arabidopsis thaliana. Plant J. 2005; 42: 890-900.

[34]

Kim YO, Kang H . The role of a zinc finger-containing glycine-rich RNA-binding protein during the cold adaptation process in Arabidopsis thaliana. Plant Cell Physiol. 2006; 47: 793-8.

[35]

Yang YF, Zhu G, Li R et al. The RNA editing factor SlORRM4 is required for normal fruit ripening in tomato. Plant Physiol. 2017; 175: 1690-702.

[36]

Hanano S, Sugita M, Sugiura M . Isolation of a novel RNA-binding protein and its association with a large ribonucleoprotein particle present in the nucleoplasm of tobacco cells. Plant Mol Biol. 1996; 31: 57-68.

[37]

Komatsu T, Mohammadi S, LSA B et al. Image analysis for a microfluidic paper-based analytical device using the CIE L*a*b* color system. Analyst. 2016; 141: 6507-9.

[38]

Luo ZD, Zhang J, Li J et al. A STAY-GREEN protein SlSGR1 regulates lycopene and β-carotene accumulation by interacting directly with SlPSY1 during ripening processes in tomato. New Phytol. 2013; 198: 442-52.

[39]

Shaul O . Unique aspects of plant nonsense-mediated mRNA decay. Trends Plant Sci. 2015; 20: 767-79.

[40]

Shaner NC, Campbell RE, Steinbach PA et al. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol. 2004; 22: 1567-72.

[41]

Duan CG, Fang YY, Zhou BJ et al. Suppression of Arabidopsis ARGONAUTE1-mediated slicing, transgene-induced RNA silencing, and DNA methylation by distinct domains of the cucumber mosaic virus 2b protein. Plant Cell. 2012; 24: 259-74.

[42]

Wu Z, Zhu D, Lin X et al. RNA binding proteins RZ-1B and RZ-1C play critical roles in regulating pre-mRNA splicing and gene expression during development in Arabidopsis. Plant Cell. 2016; 28: 55-73.

[43]

Osorio S, Scossa F, Fernie AR . Molecular regulation of fruit ripening. Front Plant Sci 2013; 4: 198.

[44]

Garcia MB, Ambat S, Adao RT Tomayto, Tomahto: a machine learning approach for tomato ripening stage identification using pixel-based color image classification. I C Humanoid Nanotec 2019, : https://WOS:000618530300146.

[45]

Sun TH, Yuan H, Cao H et al. Carotenoid metabolism in plants: the role of plastids. Mol Plant. 2018; 11: 58-74.

[46]

Tanksley SD . The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell. 2004; 16: S181-9.

[47]

Chu YH, Jang JC, Huang ZJ, et al. Tomato locule number and fruit size controlled by natural alleles of lc and fas. Plant Direct 2019; 3: e00142.

[48]

Zhang TP, Liang J, Wang M et al. Genetic engineering of the biosynthesis of glycinebetaine enhances the fruit development and size of tomato. Plant Sci. 2019; 280: 355-66.

[49]

Yuste-Lisbona FJ, Fernández-Lozano A, Pineda B et al. ENO regulates tomato fruit size through the floral meristem development network. Proc Natl Acad Sci USA. 2020; 117: 8187-95.

[50]

Wang RF, Tavano ECR, Lammers M et al. Re-evaluation of transcription factor function in tomato fruit development and ripening with CRISPR/Cas9-mutagenesis. Sci Rep 2019; 9: 1696.

[51]

Guo JE . Histone deacetylase gene SlHDT1 regulates tomato fruit ripening by affecting carotenoid accumulation and ethylene biosynthesis. Plant Sci. 2022; 318: 111235.

[52]

Ito Y, Nishizawa-Yokoi A, Endo M et al. Re-evaluation of the rin mutation and the role of RIN in the induction of tomato ripening. Nat Plants. 2017; 3: 866-74.

[53]

Gao Y, Wei W, Zhao X et al. A NAC transcription factor, NOR-like1, is a new positive regulator of tomato fruit ripening. Hortic Res 2018; 5: 75.

[54]

Wang RF, Lammers M, Tikunov Y et al. The rin, nor and Cnr spontaneous mutations inhibit tomato fruit ripening in additive and epistatic manners. Plant Sci. 2020; 294: 110436.

[55]

Li S, Xu H, Ju Z et al. The RIN-MC fusion of MADS-box transcription factors has transcriptional activity and modulates expression of many ripening genes. Plant Physiol. 2018; 176: 891-909.

[56]

Gall JG . A role for Cajal bodies in assembly of the nuclear transcription machinery. FEBS Lett. 2001; 498: 164-7.

[57]

Wang QY, Sawyer IA, Sung MH et al. Cajal bodies are linked to genome conformation. Nat Commun. 2016; 7: 10966.

[58]

Ma XL, Zhang Q, Zhu Q et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant. 2015; 8: 1274-84.

[59]

Fantini E, Falcone G, Frusciante S et al. Dissection of tomato lycopene biosynthesis through virus-induced gene silencing. Plant Physiol. 2013; 163: 986-98.

[60]

Mialoundama AS, Heintz D, Jadid N et al. Characterization of plant carotenoid cyclases as members of the flavoprotein family functioning with no net redox change. Plant Physiol. 2010; 153: 970-9.

[61]

Regnier P, Bastias J, Rodriguez-Ruiz V et al. Astaxanthin from Haematococcus pluvialis prevents oxidative stress on human endothelial cells without toxicity. Mar Drugs. 2015; 13: 2857-74.

[62]

Graewe S, Retzlaff S, Struck N et al. Going live: a comparative analysis of the suitability of the RFP derivatives RedStar, mCherry and tdTomato for intravital and in vitro live imaging of Plasmodium parasites. Biotechnol J. 2009; 4: 895-902.

[63]

Li R, Fu DQ, Zhu BZ et al. CRISPR/Cas9-mediated mutagenesis of lncRNA1459 alters tomato fruit ripening. Plant J. 2018; 94: 513-24.

[64]

Zhu BZ, Yang Y, Li R et al. RNA sequencing and functional analysis implicate the regulatory role of long non-coding RNAs in tomato fruit ripening. J Exp Bot. 2015; 66: 4483-95.

[65]

Chen XJ, Fan B, Fan C et al. First comprehensive proteome analysis of lysine crotonylation in Streptococcus agalactiae, a pathogen causing meningoencephalitis in teleosts. Proteome Sci. 2021; 19: 14.

PDF (1416KB)

67

Accesses

0

Citation

Detail

Sections
Recommended

/