Interplays between auxin and GA signaling coordinate early fruit development

Abstract

Phytohormones and their interactions are critical for fruit development and are key topics in horticulture research. Auxin, together with gibberellic acid (GA), promotes cell division and expansion, thereby regulating fruit development and enlargement after fertilization. Auxin- and GA-related mutants show parthenocarpy (fruit formation without fertilization of the ovule) in many plant species, indicating that these hormones and possibly their interactions play a key role in the regulation of fruit initiation and development. Recent studies have shown clear molecular and genetic evidence that ARF/IAA and DELLA proteins interact with one another and regulate both auxin and GA signaling pathways in response to auxin and GA during fruit growth in horticultural plants such as tomato (the most studied fleshy fruit) and strawberry (the model for Rosaceae). These recent findings provide new insights into the mechanisms by which the plant hormones auxin and GA regulate fruit development.

References

[1] Gaertner J. De Fructibus et Seminibus Plantarum . Stuttgart: typis Academiae Carolinae; 1788.

[2] Esau K. Plant Anatomy . N.Y: John Wiley and Sons Press; 1967.

[3] Weberling F . Morphology of Flowers and Inflorescences . United Kingdom: Cambridge Univ. Press; 1989.

[4] Gillaspy G, Ben-David H, Gruissem W . Fruits: a developmental perspective. Plant Cell. 1993; 5: 1439-51.

[5] Nitsch JP . Growth and morphogenesis of the strawberry as related to auxin. Am J Bot. 1950; 37: 211-5.

[6] de Jong M, Wolters-Arts M, García-Martínez J et al. The Solanum lycopersicum AUXIN RESPONSE FACTOR 7 (SlARF7) mediates cross-talk between auxin and gibberellin signaling during tomato fruit set and development. J Exp Bot. 2011; 62: 617-26.

[7] Dorcey E, Urbez C, Carbonell J et al. Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. Plant J. 2009; 58: 318-32.

[8] Liao X, Li M, Liu B et al. Interlinked regulatory loops of ABA catabolism and biosynthesis coordinate fruit growth and ripening in woodland strawberry . Proc Natl Acad Sci U S A. 2018; 115: 201812575.

[9] Ozga JA, Reinecke DM, Ayele BT et al. Developmental and hormonal regulation of gibberellin biosynthesis and catabolism in pea fruit. Plant Physiol. 2009; 150: 448-62.

[10] Knoll F. Über den Begriff «Frucht». Der Biologe. 1939; 8: 154-60.

[11] Roth I . Fruits of angiosperms . Berlin: Gebrüder Borntraeger Press; 1977.

[12] Cutler DF, Botha CEJ, Stevenson DW . Plant anatomy: An applied approach . United Kingdom: Blackwell press; 2008.

[13] Seymour GB, Østergaard L, Chapman NH et al. Fruit development and ripening. Annu Rev Plant Biol. 2013; 64: 219-41.

[14] Gasser SE, Robinson-Beers K . Pistil development. Plant Cell. 1993; 5: 1231-9.

[15] Pabon-Mora N, Litt A . Comparative anatomical and developmental analysis of dry and fleshy fruits of Solanaceae. Am J Bot. 2011; 98: 1415-36.

[16] Ho LC, Hewitt JD . Fruit development. In: Atherton, JG and Rudich J eds. The Tomato Crop.NY: Chapman and Hall; 1986; 201-39.

[17] Hollender CA, Geretz AC, Slovin JP et al. Flower and early fruit development in a diploid strawberry. Fragaria vesca Planta. 2011; 235: 1123-39.

[18] Conde C, Silva PF, Dias ACP et al. Biochemical changes throughout grape berry development and fruit and wine quality. Food Review. 2007; 1: 1-22.

[19] Archbold DD, Dennis FG . Strawberry receptacle growth and endogenous IAA content as affected by growth regulator application and achene removal. J Am Soc Hortic Sci. 1985; 110: 816-20.

[20] Picken AJF . A review of pollination and fruit set in the tomato (Lycopersicon esculentum mill.). Journal of Horticultural Science. 1984; 59: 1-13.

[21] Gustafson FG . Inducement of fruit development by growth-promoting chemicals. Proc Natl Acad Sci U S A. 1936; 22: 628-36.

[22] Gustafson FG . The natural cause of parthenocarpy. Am J Bot. 1939; 26: 135-8.

[23] Nitsch JP . Growth and morphogenesis of the strawberry as related to auxin. Am J Bot. 1950; 37: 211-5.

[24] Nitsch JP . Plant hormones in the development of fruit. Q Rev Biol. 1952; 27: 33-57.

[25] Gorguet B, van Heusden AW, Lindhout P . Parthenocarpic fruit development in tomato. Plant Biol. 2005; 7: 131-9.

[26] Kang C, Darwish O, Geretz A et al. Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca . Plant Cell. 2013; 25: 1960-78.

[27] Cheng C, Jiao C, Singer et al. Gibberellin-induced changes in the transcriptome of grapevine (Vitis labrusca × V. vinifera) cv. Kyoho flowers. BMC Genomics. 2015; 16: 128.

[28] Gouthu S, Deluc LG . Timing of ripening initiation in grape berries and its relationship to seed content and pericarp auxin levels. BMC Plant Biol. 2015; 15: 46.

[29] Upadhyay A, Jogaih S, Kadoo N et al. Expression of stable reference genes and SPINDLY gene in response to gibberellic acid application at different stages of grapevine development. Biologia plantarum. 2015; 59: 436-44.

[30] McAtee P, Karim S, Schaffer R et al. Dynamic interplay between phytohormones is required for fruit development, maturation, and ripening . Front Plant Sci. 2013; 4: 79.

[31] Dharmasiri N, Dharmasiri S, Estelle M . The F-box protein TIR1 is an auxin receptor. Nature. 2005; 435: 441-5.

[32] Kepinski S, Leyser O . The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature. 2005; 435: 446-51.

[33] Mockaitis K, Estelle M . Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol. 2008; 24: 55-80.

[34] Salehin M, Bagchi R, Estelle M . SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development. Plant Cell. 2015; 27: 9-19.

[35] Ulmasov T, Hagen G, Guilfoyle TJ . Dimerization and DNA binding of auxin response factors. Plant J. 1999a; 19: 309-19.

[36] Ulmasov T, Hagen G, Guilfoyle TJ . Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci U S A. 1999b; 96: 5844-9.

[37] Vivian-Smith A, Adam. The molecular basis for the initiation of fruit development and parthenocarpy. Theses. 2001.

[38] Goetz M, Vivian-Smith A, Johnson SD et al. AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis . Plant Cell. 2006; 18: 1873-86.

[39] Davière JM, Achard P . A pivotal role of DELLAs in regulating multiple hormone signals. Mol Plant. 2016; 9: 10-20.

[40] de Lucas M, Daviere JM, Rodriguez-Falcon M et al. A molecular framework for light and gibberellin control of cell elongation. Nature. 2008; 451: 480-4.

[41] Peng J, Carol P, Richards DE et al. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev. 1997; 11: 3194-205.

[42] Silverstone AL, Ciampaglio CN, Sun TP . The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell. 1998; 10: 155-69.

[43] Sun TP . Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant Physiol. 2010; 154: 567-70.

[44] Mcginnis KM, Thomas SG, Soule JD et al. The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell. 2003; 15: 1120-30.

[45] Murase K, Hirano Y, Sun TP et al. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature. 2008; 456: 459-63.

[46] Ueguchi-Tanaka M, Ashikari M, Nakajima M et al. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature. 2005; 437: 693-8.

[47] Fuentes S, Ljung K, Sorefan K et al. Fruit growth in Arabidopsis occurs via DELLA-dependent and DELLA-independent gibberellin responses. Plant Cell. 2012; 24: 3982-96.

[48] Serrani JC, Fos M, Atarés A et al. Effect of gibberellin and auxin on parthenocarpic fruit growth induction in the cv micro-tom of tomato. J Plant Growth Regul. 2007; 26: 211-21.

[49] Frigerio M, Alabadi D, Perez-Gomez J et al. Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol. 2006; 142: 553-63.

[50] Ross JJ, O’Neill DP, Smith JJ et al. Evidence that auxin promotes gibberellin A1 biosynthesis in pea. Plant J. 2000; 21: 547-52.

[51] Wolbang CM, Chandler PM, Smith JJ et al. Auxin from the developing inflorescence is required for the biosynthesis of active gibberellins in barley stems. Plant Physiol. 2004; 134: 769-76.

[52] Wolbang CM, Ross JJ . Auxin promotes gibberellin biosynthesis in decapitated tobacco plants. Planta. 2001; 214: 153-7.

[53] Hu J, Alon I, Naomi O et al. The interaction between DELLA and ARF/IAA mediates crosstalk between gibberellin and auxin signaling to control fruit initiation in tomato. Plant Cell. 2018; 30: 1710-28.

[54] Fu X, Harberd NP. Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature. 2003;421:740-3.

[55] Wang H, Jones B, Li Z et al. The tomato aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell. 2005; 17: 2676-92.

[56] Zhang JH, Chen R, Xio J et al. A single-base deletion mutation in SlIAA9 gene causes tomato (Solanum lycopersicum) entire mutant . J Plant Res. 2007; 120: 671-8.

[57] de Jong M, Wolters-Arts M, Feron R et al. Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development . Plant J. 2009; 57: 160-70.

[58] Vriezen WH, Feron R, Maretto F et al. Changes in tomato ovary transcriptome demonstrate complex hormonal regulation of fruit set. New Phytol. 2008; 177: 60-76.

[59] Serrani JC, Ruiz-Rivero O, Fos M et al. Auxin-induced fruit-set in tomato is mediated in part by gibberellins. Plant J. 2008; 56: 922-34.

[60] Carrera E, Ruiz-Rivero O, Peres LE et al. Characterization of the procera tomato mutant shows novel functions of the SIDELLA protein in the control of flower morphology, cell division and expansion, and the auxin-signaling pathway during fruit-set and development. Plant Physiol. 2012; 160: 1581-96.

[61] Oh E, Zhu JY, Bai MY et al. Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. elife. 2014; 3: e03031.

[62] Ding J, Chen B, Xia X et al. Cytokinin-induced parthenocarpic fruit development in tomato is partly dependent on enhanced gibberellin and auxin biosynthesis. PLoS One. 2013; 8: e70080.

[63] Breitel DA, Chappell-Maor L, Meir S et al. AUXIN RESPONSE FACTOR 2 intersects hormonal signals in the regulation of tomato fruit ripening. PLoS Genet. 2016; 12: e1005903.

[64] Zhang X, Yan F, Tang Y 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. 2015; 56: 2110-24.

[65] Sagar M, Chervin C, Mila I et al. SlARF4, an auxin response factor involved in the control of sugar metabolism during tomato fruit development . Plant Physiol. 2013; 161: 1362-74.

[66] Liu S, Zhang Y, Feng Q et al. Tomato AUXIN RESPONSE FACTOR 5 regulates fruit set and development via the mediation of auxin and gibberellin signaling. Sci Rep. 2018; 8: 2971.

[67] Yuan Y, Xu X, Gong Z et al. Auxin response factor 6A regulates photosynthesis, sugar accumulation, and fruit development in tomato. Hortic Res. 2019; 6: 85.

[68] Goetz M, Hooper LC, Johnson SD et al. Expression of aberrant forms of AUXIN RESPONSE FACTOR8 stimulates parthenocarpy in Arabidopsis and tomato . Plant Physiol. 2007; 145: 351-66.

[69] de Jong M, Wolter-Arts M, Schimmel BCJ et al. Solanum lycopersicum AUXIN RESPONSE FACTOR 9 regulates cell division activity during early tomato fruit development . J Exp Bot. 2015; 66: 3405-16.

[70] Yuan Y, Mei L, Wu M et al. SlARF10, an auxin response factor, is involved in chlorophyll and sugar accumulation during tomato fruit development. J Exp Bot. 2018; 69: 5507-18.

[71] Chaabouni S, Jones B, Delalande C et al. Sl-IAA3, a tomato aux/IAA at the crossroads of auxin and ethylene signalling involved in differential growth. J Exp Bot. 2009; 60: 1349-62.

[72] Liu M, Chen Y, Chen Y et al. The tomato ethylene response factor Sl-ERF.B3 integrates ethylene and auxin signaling via direct regulation of Sl-aux/IAA27 . New Phytol. 2018; 219: 631-40.

[73] Zhou J, Sittmann J, Guo L et al. Gibberellin and auxin signaling genes RGA1 and ARF8 repress accessory fruit initiation in diploid strawberry. Plant Physiol. 2021; 185: 1059-75.

[74] Harpster MH, Brummell DA, Dunsmuir P . Expression analysis of a ripening-specific, auxin-repressed endo-1, 4-beta-glucanase gene in strawberry. Plant Physiol. 1998; 118: 1307-16.

[75] Aharoni A, Keizer LCP, Blanco-Portales R et al. Novel insight into vascular, stress, and auxin-dependent and -independent gene expression programs in strawberry, a non-climacteric fruit. Plant Physiol. 2002; 129: 1019-31.

[76] Feng J, Dai C, Luo H et al. Reporter gene expression reveals precise auxin synthesis sites during fruit and root development in wild strawberry. J Exp Bot. 2019; 70: 563-74.

[77] Mazzoni-Putman SM, Brumos J, Zhao C et al. Auxin interactions with other hormones in plant development. Cold Spring Harb Perspect Biol. 2021; 13.

[78] Caruana JC, Sittmann JW, Wang W et al. Suppressor of Runnerless encodes a DELLA protein that controls runner formation for asexual reproduction in strawberry. Mol Plant. 2018; 11: 230-3.

[79] Sugiura A, Inaba A . Studies on the mechanism of gibberellin-induced seedlessness of Delaware grapes. I. Effect of pre-bloom gibberellin treatment on pollen germination. Engei Gakkai Zasshi. 1966; 35: 233-41.

[80] Kimura PH, Okamoto G, Hirano K . Effects of gibberellic acid and streptomycin on pollen germination and ovule and seed development in Muscat bailey a. Am J Enol Viticult. 1996; 47: 152-6.

[81] Agüero C, Vigliocco A, Abdala G et al. Effect of gibberellic acid and uniconazol on embryo abortion in the stenospermocarpic grape cultivars Emperatriz and Perlon. Plant Growth Regul. 2000; 30: 9-16.

[82] Acheampong AK, Zheng C, Halaly T et al. Abnormal endogenous repression of GA signaling in a seedless table grape cultivar with high berry growth response to GA application. Front Plant Sci. 2017; 8: 850.

[83] He H, Liang G, Lu S et al. Genome-wide identification and expression analysis of GA2ox, GA3ox, and GA20ox are related to gibberellin oxidase genes in grape (Vitis Vinifera L.) . Genes. 2019; 10: 680.

[84] Wang W, Bai Y, Koilkonda P et al. Genome-wide identification and characterization of gibberellin metabolic and signal transduction (GA MST) pathway mediating seed and berry development (SBD) in grape (Vitis vinifera L.). BMC Plant Biol. 2020; 20: 384.

[85] Weaver RJ, Mccune SB . Further studies with gibberellin on Vitis vinifera grapes. Bot Gaz. 1960; 121: 155-62.

[86] Lu L, Liang J, Zhu X et al. Auxin- and cytokinin-induced berries set in grapevine partly rely on enhanced gibberellin biosynthesis. Tree Genet Genomes. 2016;12:41.

[87] Parada F, Espinoza C, Arce-Johnson P . InTech. In: El-Esawi M, ed. Phytohormones-Signaling Mechanisms and Crosstalk in Plant Development and Stress Responses . USA: InRech press, 2017.

[88] Gogoy F, Kuhn N, Muñoz M et al. The role of auxin during early berry development in grapevine as revealed by transcript profiling from pollination to fruit set. Hortic Res. 2021; 8: 140.

[89] Jung CJ, Hur YY, Yu HJ et al. Gibberellin application at pre-bloom in grapevines Down-regulates the expressions of VvIAA9 and VvARF7, negative regulators of fruit set initiation, during Parthenocarpic fruit development . PLoS One. 2014; 9: e95634.

[90] Wang C, Jogaiah S, Zhang W et al. Spatio-temporal expression of miRNA159 family members and their GAMYB target gene during the modulation of gibberellin-induced grapevine parthenocarpy. J Exp Bot. 2018; 69: 3639-50.

[91] Weiss D, Ori N . Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol. 2007; 144: 1240-6.

[92] Bai MY, Shang JX, Oh E et al. Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol. 2012; 14: 810-7.

[93] Hou X, Li Y, Xia K et al. DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell. 2010; 19: 884-94.