Auxin response factor 6A regulates photosynthesis, sugar accumulation, and fruit development in tomato

Yujin Yuan , Xin Xu , Zehao Gong , Yuwei Tang , Mengbo Wu , Fang Yan , Xiaolan Zhang , Qian Zhang , Fengqing Yang , Xiaowei Hu , Qichen Yang , Yingqing Luo , Lihua Mei , Wenfa Zhang , Cai-Zhong Jiang , Wangjin Lu , Zhengguo Li , Wei Deng

Horticulture Research ›› 2019, Vol. 6 ›› Issue (1) : 85

PDF (2862KB)
Horticulture Research ›› 2019, Vol. 6 ›› Issue (1) :85 DOI: 10.1038/s41438-019-0167-x
Article
research-article
Auxin response factor 6A regulates photosynthesis, sugar accumulation, and fruit development in tomato
Author information +
History +
PDF (2862KB)

Abstract

Auxin response factors (ARFs) are involved in auxin-mediated transcriptional regulation in plants. In this study, we performed functional characterization of SlARF6A in tomato. SlARF6A is located in the nucleus and exhibits transcriptional activator activity. Overexpression of SlARF6A increased chlorophyll contents in the fruits and leaves of tomato plants, whereas downregulation of SlARF6A decreased chlorophyll contents compared with those of wild-type (WT) plants. Analysis of chloroplasts using transmission electron microscopy indicated increased sizes of chloroplasts in SlARF6A-overexpressing plants and decreased numbers of chloroplasts in SlARF6A-downregulated plants. Overexpression of SlARF6A increased the photosynthesis rate and accumulation of starch and soluble sugars, whereas knockdown of SlARF6A resulted in opposite phenotypes in tomato leaves and fruits. RNA-sequence analysis showed that regulation of SlARF6A expression altered the expression of genes involved in chlorophyll metabolism, photosynthesis and sugar metabolism. SlARF6A directly bound to the promoters of SlGLK1, CAB, and RbcS genes and positively regulated the expression of these genes. Overexpression of SlARF6A also inhibited fruit ripening and ethylene production, whereas downregulation of SlARF6A increased fruit ripening and ethylene production. SlARF6A directly bound to the SAMS1 promoter and negatively regulated SAMS1 expression. Taken together, these results expand our understanding of ARFs with regard to photosynthesis, sugar accumulation and fruit development and provide a potential target for genetic engineering to improve fruit nutrition in horticulture crops.

Cite this article

Download citation ▾
Yujin Yuan, Xin Xu, Zehao Gong, Yuwei Tang, Mengbo Wu, Fang Yan, Xiaolan Zhang, Qian Zhang, Fengqing Yang, Xiaowei Hu, Qichen Yang, Yingqing Luo, Lihua Mei, Wenfa Zhang, Cai-Zhong Jiang, Wangjin Lu, Zhengguo Li, Wei Deng. Auxin response factor 6A regulates photosynthesis, sugar accumulation, and fruit development in tomato. Horticulture Research, 2019, 6 (1) : 85 DOI:10.1038/s41438-019-0167-x

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Klee, H. J. & Giovannoni, J. J. Genetics and control of tomato fruit ripening and quality attributes. Annu. Rev. Genet. 45, 41-59 (2011).

[2]

Ho, L. C. & Hewitt, J. D. Fruit development. (eds. Atherton, J. G. & Rudich, J.) The Tomato Crop. 201-240 (Chapman and Hall, London, 1986).

[3]

Schaffer, A. A. & Petreikov, M. Sucrose-to-starch metabolism in tomato fruit undergoing transient starch accumulation. Plant Physiol. 113, 739-746 (1997).

[4]

Nadakuduti, S. S., Holdsworth, W. L., Klein, C. L. & Barry, C. S. KNOX genes influence a gradient of fruit chloroplast development through regulation of GOLDEN2-LIKE expression in tomato. Plant J. 78, 1022-1033 (2014).

[5]

Kolotilin, I. et al. Transcriptional profiling of high pigment 2(dg) tomato mutant links early fruit plastid biogenesis with its overproduction of phytonutrients. Plant Physiol. 145, 389-401 (2007).

[6]

Rohrmann, J. et al. Combined transcription factor profiling, microarray analysis and metabolite profiling reveals the transcriptional control of metabolic shifts occurring during tomato fruit development. Plant J. 68, 999-1013 (2011).

[7]

Waters, M. T., Moylan, E. C. & Langdale, J. A. GLK transcription factors regulate chloroplast development in a cell-autonomous manner. Plant J. 56, 432-444 (2008).

[8]

Nguyen, C. V. et al. Tomato Golden 2-like (GLK) transcription factors reveal molecular gradients functioning during fruit development and ripening. Plant Cell 26, 585-601 (2014).

[9]

Pan, Y. et al. Network inference analysis identifies an APRR2-like gene linked to pigment accumulation in tomato and pepper fruits. Plant Physiol. 161, 1476-1485 (2013).

[10]

Meng, L. H. et al. BEL1-LIKE HOMEODOMAIN11 regulates chloroplast development and chlorophyll synthesis in tomato fruit. Plant J. 94, 1126-1140 (2018).

[11]

Li, S. et al. The RIN-MC fusion of MADS-box transcription factors has transcriptional activity and modulates expression of many ripening genes. Plant Physiol. 176, 891-909 (2018).

[12]

Gao, Y. et al. A NAC transcription factor, NOR-like1, is a new positive regulator of tomato fruit ripening. Hortic. Res. 5, 75 (2018).

[13]

Roje, S . S-Adenosyl-L-methionine: beyond the universal methyl group donor. Phytochemistry 67, 1686-1698 (2006).

[14]

Barry, C. S., Llop-Tous, M. I. & Grierson, D. The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol. 123, 979-986 (2000).

[15]

Manning, K. et al. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 38, 948-952 (2006).

[16]

Itkin, M. et al. TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant J. 60, 1081-1095 (2009).

[17]

Chung, M. Y. et al. A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J. 64, 936-947 (2010).

[18]

Karlova, R. et al. Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23, 923-941 (2011).

[19]

Bemer, M. et al. The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-independent aspects of fruit ripening. Plant Cell 24, 4437-4451 (2012).

[20]

Gao, Y. et al. Diversity and redundancy of the ripening regulatory networks revealed by the fruitENCODE and the new CRISPR/Cas9 CNR and NOR mutants. Hortic. Res. 6, 39 (2019).

[21]

Liu, M. et al. The chimeric repressor version of an Ethylene Response Factor (ERF) family member, Sl-ERF.B3, shows contrasting effects on tomato fruit ripening. New Phytol. 203, 206-218 (2014a).

[22]

De Jong, M., Wolters-Arts, M., Feron, R., Mariani, C. & Vriezen, W. H. The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J. 57, 160-170 (2009).

[23]

Devoghalaere, F. et al. A genomics approach to understanding the role of auxin in apple (Malus x domestica) fruit size control. BMC Plant Biol. 12, 7 (2012).

[24]

Ulmasov, T., Hagen, G. & Guifoyle, T. Dimerization and DNA binding of auxin response factors. Plant J. 19, 309-319 (1999).

[25]

Guilfoyle, T. J. & Hagen, G. Auxin response factors. Curr. Opin. Plant. Biol. 10, 453-460 (2007).

[26]

Guilfoyle, T. J. & Hagen, G. Getting a grasp on domain III/IV responsible for Auxin Response Factor-IAA protein interactions. Plant Sci. 190, 82-88 (2012).

[27]

Zouine, M. et al. Characterization of the tomato ARF gene family uncovers a multi-levels post-transcriptional regulation including alternative splicing. PLoS ONE 9, e84203 (2014).

[28]

Wang, Y. et al. Diversification, phylogeny and evolution of auxin response factor (ARF) family: insights gained from analyzing maize ARF genes. Mol. Biol. Rep. 39, 2401-2415 (2012).

[29]

Guan, X. X. et al. Temporal and spatial distribution of auxin response factor genes during tomato flower abscission. J. Plant. Growth Regul. 33, 17-327 (2013).

[30]

Liu, X. et al. AUXIN RESPONSE FACTOR 3 integrates the functions of AGAMOUS and APETALA2 in floral meristem determinacy. Plant J. 80, 629-641 (2014b).

[31]

Ckurshumova, W., Smirnova, T., Marcos, D., Zayed, Y. & Berleth, T. Irrepressible MONOPTEROS/ARF5 promotes de novo shoot formation. New Phytol. 204, 556-566 (2014).

[32]

Zhang, X. L. et al. Auxin response gene SlARF3 plays multiple roles in tomato development and is involved in the formation of epidermal cells and trichomes. Plant Cell Physiol. 56, 2110-2124 (2015).

[33]

Jones, B. et al. Down-regulation of DR12, an auxin-response-factor homolog, in the tomato results in a pleiotropic phenotype including dark green and blotchy ripening fruit. Plant J. 32, 603-613 (2002).

[34]

Sagar, M. et al. Sl-ARF4, an auxin response factor involved in the control of sugar metabolism during tomato fruit development. Plant Physiol. 161, 1362-1374 (2013).

[35]

Yuan, Y. J. et al. SlARF10, an auxin response factor, is involved in chlorophyll and sugar accumulation during tomato fruit development. J. Exp. Bot. 69, 5507-5518 (2018).

[36]

Liu, N. et al. Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. J. Exp. Bot. 65, 2507-2520 (2014).

[37]

Krogan, N. T., Ckurshumova, W., Marcos, D., Caragea, A. E. & Berleth, T. Deletion of MP/ARF5 domains III and IV reveals a requirement for Aux/IAA regulation in Arabidopsis leaf vascular patterning. New Phytol. 194, 391-401 (2011).

[38]

Kobayashi, K. et al. Regulation of root greening by light and auxin/cytokinin signaling in Arabidopsis. Plant Cell 24, 1081-1095 (2012).

[39]

Powell, A. L. T. et al. Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336, 1711-1715 (2012).

[40]

Jansson, S. The light-harvesting chlorophyll a/b-binding proteins. BBA-Biomembr. 1184, 1-19 (1994).

[41]

Patel, M. & Berry, J. O. Rubisco gene expression in C4 plants. J. Exp. Bot. 59, 1625-1634 (2008).

[42]

Spreitzer, M. E. & Salvucci, R. J. Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Ann. Rev. Plant Biol. 53, 449-475 (2002).

[43]

Sasanuma, T. Characterization of the rbcS multigene family in wheat: sub-family classification, determination of chromosomal location and evolutionary analysis. Mol. Gen. Genet. 265, 161-171 (2001).

[44]

Stark, D. M., Timmerman, K. P., Barry, G. F., Preiss, J. & Kishore, G. M. Regulation of the amount of starch in plant tissues by ADP glucose pyrophosphorylase. Science 258, 287-292 (1992).

[45]

Yin, Y. G. et al. Salinity induces carbohydrate accumulation and sugar-regulated starch biosynthetic genes in tomato (Solanum lycopersicum L. cv.‘Micro-Tom’) fruits in an ABA-and osmotic stress-independent manner. J. Exp. Bot. 61, 563-574 (2009).

[46]

Tiessen, A. et al. Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: A noble regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14, 2191-2213 (2002).

[47]

Sauter, M., Moffatt, B., Saechao, M. C., Hell, R. & Wirtz, M. Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis. Biochem. J. 451, 145-154 (2013).

[48]

Schaffer, A. A. et al. ADP glucose pyrophosphorylase activity and starch accumulation in immature tomato fruit: the effect of a Lycopersicon hirsutum-derived introgression encoding for the large subunit. Plant Sci. 152, 135-144 (2000).

[49]

Baxter, C. J. et al. Fruit carbohydrate metabolism in an introgression of tomato with increased fruit soluble solids. Plant Cell Physiol. 46, 425-437 (2005).

[50]

Breitel, D. A. et al. AUXIN RESPONSE FACTOR 2 intersects hormonal signals in the regulation of tomato fruit ripening. PLoS. Genet. 12, e1005903 (2016).

[51]

Wang, K. L., Li, H. & Ecker, J. R. Ethylene biosynthesis and signaling networks. Plant Cell 14, S131-S151 (2002).

[52]

Yang, S. F. & Hoffman, N. E. Ethylene biosynthesis and its regulation in higher plants. Ann. Rev. Plant Physiol. 35, 155-189 (1984).

[53]

Van de Poel, B. et al. Targeted systems biology profiling of tomato fruit reveals coordination of the Yang cycle and a distinct regulation of ethylene biosynthesis during post-climacteric ripening. Plant Physiol. 160, 1498-1514 (2012b).

[54]

Mao, D. et al. FERONIA receptor kinase interacts with S-adenosylmethionine synthetase and suppresses S-adenosylmethionine production and ethylene biosynthesis in Arabidopsis. Plant Cell Environ. 38, 2566-2574 (2015).

[55]

Gong, B. et al. Overexpression of S-adenosyl-L-methionine synthetase increased tomato tolerance to alkali stress through polyamine metabolism. Plant Biotechnol. J. 12, 694-708 (2014).

[56]

Ruzicka, K. et al. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19, 2197-2212 (2007).

[57]

Stepanova, A. N., Yun, J., Likhacheva, A. V. & Alonso, J. M. Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19, 2169-2185 (2007).

[58]

Muday, G. K., Rahman, A. & Binder, B. M. Auxin and ethylene: collaborators or competitors?. Trends Plant. Sci. 17, 181-195 (2012).

[59]

Liu, M. et al. The tomato Ethylene Response Factor Sl-ERF.B3 integrates ethylene and auxin signaling via direct regulation of Sl-Aux/IAA27. New Phytol. 219, 631-640 (2018).

[60]

Chaabouni, S. et al. Sl-IAA3, a tomato Aux/IAA at the crossroads of auxin and ethylene signaling involved in differential growth. J. Exp. Bot. 60, 1349-1362 (2009).

[61]

Maury, P., Mojayad, F., Berger, M. & Planchon, C. Photochemical response to drought acclimation in two sunflower genotypes. Physiol. Plant. 98, 57-66 (1996).

[62]

Geigenberger, P., Lerchi, J., Stitt, M. & Sonnewald, U. Phloem-specific expression of pyrophosphatase inhibits long distance transport of carbohydrates and amino acids in tobacco plants. Plant Cell Environ. 19, 43-55 (1996).

[63]

Hellens, R. P. et al. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant. Methods 1, 13 (2005).

[64]

Han, Y. C. et al. Banana transcription factor MaERF11 recruits histone deacetylase MaHDA1 and represses the expression of MaACO1 and expansins during fruit ripening. Plant Physiol. 171, 1070-1084 (2016).

[65]

Qin, G., Wang, Y., Cao, B., Wang, W. & Tian, S. Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening. Plant J. 70, 243-255 (2012).

PDF (2862KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/