Molecular and genetic regulations of fleshy fruit shape and lessons from Arabidopsis and rice

Abstract

Fleshy fruit shape is an important external quality trait influencing the usage of fruits and consumer preference. Thus, modification of fruit shape has become one of the major objectives for crop improvement. However, the underlying mechanisms of fruit shape regulation are poorly understood. In this review we summarize recent progress in the genetic basis of fleshy fruit shape regulation using tomato, cucumber, and peach as examples. Comparative analyses suggest that the OFP-TRM (OVATE Family Protein - TONNEAU1 Recruiting Motif) and IQD (IQ67 domain) pathways are probably conserved in regulating fruit shape by primarily modulating cell division patterns across fleshy fruit species. Interestingly, cucumber homologs of FRUITFULL (FUL1), CRABS CLAW (CRC) and 1-aminocyclopropane-1-carboxylate synthase 2 (ACS2) were found to regulate fruit elongation. We also outline the recent progress in fruit shape regulation mediated by OFP-TRM and IQD pathways in Arabidopsis and rice, and propose that the OFP-TRM pathway and IQD pathway coordinate regulate fruit shape through integration of phytohormones, including brassinosteroids, gibberellic acids, and auxin, and microtubule organization. In addition, functional redundancy and divergence of the members of each of the OFP, TRM, and IQD families are also shown. This review provides a general overview of current knowledge in fruit shape regulation and discusses the possible mechanisms that need to be addressed in future studies.

Acknowledgements

This work was supported by the Natural Science Foundation of Hebei Province (C2021204015), the 2021 Project for the Introduction of Oversea Students in Hebei Province (C20210510), science and technology research projects of colleges and universities in Hebei Province (ZD2022111), the Introduction of Talents Start-up fund of the State Key Laboratory of North China Crop Improvement and Regulation (NCCIR2020RC-13), the Introduction of Talents Start-up fund of Hebei Agricultural University (YJ2020067), the Hebei Fruit Vegetables Seed Industry Science and Technology Innovation Team Project (21326309D), and the Vegetable Innovation Team Project of Hebei Modern Agricultural Industrial Technology System (HBCT2018030203).

Conflict of interest

The authors declare no conflicts of interest.

References

[1] Liu Z, Ma H, Jung S et al. Developmental mechanisms of fleshy fruit diversity in Rosaceae. Annu Rev Plant Biol. 2020; 71: 547-73.

[2] Gomez MD, Vera-Sirera F, Perez-Amador MA . Molecular programme of senescence in dry and fleshy fruits. J Exp Bot. 2014; 65: 4515-26.

[3] Lorts C, Briggeman T, Sang T . Evolution of fruit types and seed dispersal: a phylogenetic and ecological snapshot. J Syst Evol. 2008; 46: 396-404.

[4] van der Knaap E, Østergaard L . Shaping a fruit: developmental pathways that impact growth patterns. Semin Cell Dev Biol. 2018; 79: 27-36.

[5] Rodriguez GR, Munos S, Anderson C et al. Distribution of SUN, OVATE, LC, and FAS in the tomato germplasm and the relationship to fruit shape diversity. Plant Physiol. 2011; 156: 275-85.

[6] Wu S, Zhang B, Keyhaninejad N et al. A common genetic mechanism underlies morphological diversity in fruits and other plant organs. Nat Commun. 2018; 9: 4734.

[7] Pan Y, Wang Y, McGregor C et al. Genetic architecture of fruit size and shape variation in cucurbits: a comparative perspective. Theor Appl Genet. 2020; 133: 1-21.

[8] Liu Z, Franks RG . Molecular basis of fruit development. Front Plant Sci. 2015; 6: 28.

[9] Dong Y, Ostergaard L . Fruit development and diversification. Curr Biol. 2019; 29: R781-5.

[10] Mauxion J-P, Chevalier C, Gonzalez N . Complex cellular and molecular events determining fruit size. Trends Plant Sci. 2021; 26: 1023-38.

[11] Quinet M, Angosto T, Yuste-Lisbona FJ et al. Tomato fruit development and metabolism. Front Plant Sci. 2019; 10: 1554.

[12] Cirilli M, Baccichet I, Chiozzotto R et al. Genetic and phenotypic analyses reveal major quantitative loci associated to fruit size and shape traits in a non-flat peach collection (P. persica L. Batsch). Hortic Res. 2021; 8: 232.

[13] Visa S, Cao C, Gardener BM et al. Modeling of tomato fruits into nine shape categories using elliptic Fourier shape modeling and Bayesian classification of contour morphometric data. Euphytica. 2014; 200: 429-39.

[14] Quispe-Choque G, Rojas-Ledezma S, Maydana-Marca A . Morphological diversity determination of the tomato fruit collection (Solanum lycopersicum L.) by phenotyping based on digital images. J Selva Andina Res Soc. 2022; 13: 51-68.

[15] Schwarz D, Thompson AJ, Kläring H-P . Guidelines to use tomato in experiments with a controlled environment. Front Plant Sci. 2014; 5: 625.

[16] Liu X, Pan Y, Liu C et al. Cucumber fruit size and shape variations explored from the aspects of morphology, histology, and endogenous hormones. Plants. 2020; 9: 772.

[17] Guo J, Cao K, Li Y et al. Comparative transcriptome and microscopy analyses provide insights into flat shape formation in peach (Prunus persica). Front Plant Sci. 2017; 8: 2215.

[18] Li P, Chen YH, Lu J et al. Genes and their molecular functions determining seed structure, components, and quality of rice. Rice (N Y). 2022; 15: 18.

[19] Grandillo S, Ku H, Tanksley S . Identifying the loci responsible for natural variation in fruit size and shape in tomato. Theor Appl Genet. 1999; 99: 978-87.

[20] Gonzalo MJ, Van Der Knaap E . A comparative analysis into the genetic bases of morphology in tomato varieties exhibiting elongated fruit shape. Theor Appl Genet. 2008; 116: 647-56.

[21] Sierra-Orozco E, Shekasteband R, Illa-Berenguer E et al. Identification and characterization of GLOBE, a major gene controlling fruit shape and impacting fruit size and marketability in tomato. Hortic Res. 2021; 8: 138.

[22] Rodriguez GR, Kim HJ, van der Knaap E . Mapping of two suppressors of OVATE (sov) loci in tomato. Heredity (Edinb). 2013; 111: 256-64.

[23] Wu S, Xiao H, Cabrera A et al. SUN regulates vegetative and reproductive organ shape by changing cell division patterns. Plant Physiol. 2011; 157: 1175-86.

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

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

[26] Yuste-Lisbona FJ, Fernandez-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.

[27] Lippman Z, Tanksley SD . Dissecting the genetic pathway to extreme fruit size in tomato using a cross between the small-fruited wild species Lycopersicon pimpinellifolium and L. esculentum var. Giant Heirloom. Genetics (Austin). 2001; 158: 413-22.

[28] Xu C, Liberatore KL, MacAlister CA et al. A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat Genet. 2015; 47: 784-92.

[29] Muños S, Ranc N, Botton E et al. Increase in tomato locule number is controlled by two single-nucleotide polymorphisms located near WUSCHEL. Plant Physiol. 2011; 156: 2244-54.

[30] Rodriguez-Leal D, Lemmon ZH, Man J et al. Engineering quantitative trait variation for crop improvement by genome editing. Cell. 2017; 171: 470-480.e8.

[31] Lecomte L, Saliba-Colombani V, Gautier A et al. Fine mapping of QTLs of chromosome 2 affecting the fruit architecture and composition of tomato. Mol Breed. 2004; 13: 1-14.

[32] van der Knaap E, Chakrabarti M, Chu YH et al. What lies beyond the eye: the molecular mechanisms regulating tomato fruit weight and shape. Front Plant Sci. 2014; 5: 227.

[33] Somssich M, Je BI, Simon R et al. CLAVATA-WUSCHEL signaling in the shoot meristem. Development. 2016; 143: 3238-48.

[34] Xiao H, Jiang N, Schaffner E et al. A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science. 2008; 319: 1527-30.

[35] Liu J, Van Eck J, Cong B et al. A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. Proc Natl Acad Sci USA. 2002; 99: 13302-6.

[36] Grandillo S, Ku H-M, Tanksley SD . Characterization of fs8.1, a major QTL influencing fruit shape in tomato. Mol Breed. 1996; 2: 251-60.

[37] Sun L, Rodriguez GR, Clevenger JP et al. Candidate gene selection and detailed morphological evaluations of fs8.1, a quantitative trait locus controlling tomato fruit shape. J Exp Bot. 2015; 66: 6471-82.

[38] Wang Y, Clevenger JP, Illa-Berenguer E et al. A comparison of sun, ovate, fs8.1 and auxin application on tomato fruit shape and gene expression. Plant Cell Physiol. 2019; 60: 1067-81.

[39] Snouffer A, Kraus C, van der Knaap E . The shape of things to come: ovate family proteins regulate plant organ shape. Curr Opin Plant Biol. 2020; 53: 98-105.

[40] Wu S, Clevenger JP, Sun L et al. The control of tomato fruit elongation orchestrated by sun, ovate and fs8.1 in a wild relative of tomato. Plant Sci. 2015; 238: 95-104.

[41] Lazzaro MD, Wu S, Snouffer A et al. Plant organ shapes are regulated by protein interactions and associations with microtubules. Front Plant Sci. 2018; 9: 1766.

[42] Zhang B, Li Q, Keyhaninejad N et al. A combinatorial TRM-OFP module bilaterally fine-tunes tomato fruit shape. New Phytol. 2023; 238: 2393-409.

[43] Yang B, Wendrich JR, De Rybel B et al. Rice microtubule-associated protein IQ67-DOMAIN14 regulates grain shape by modulating microtubule cytoskeleton dynamics. Plant Biotechnol J. 2020; 18: 1141-52.

[44] Wendrich JR, Yang B-J, Mijnhout P et al. IQD proteins integrate auxin and calcium signaling to regulate microtubule dynamics during Arabidopsis development. bioRxiv. 2018.

[45] Fenn MA, Giovannoni JJ . Phytohormones in fruit development and maturation. Plant J. 2021; 105: 446-58.

[46] Sharif R, Su L, Chen X et al. Involvement of auxin in growth and stress response of cucumber. Veg Res. 2022; 2: 13.

[47] Kong X, He M, Guo Z et al. microRNA regulation of fruit development, quality formation and stress response. Fruit Res. 2021; 1: 1-11.

[48] Carvalho A, Vicente MH, Ferigolo LF et al. miR319-targeted CP4/LANCEOLATE directly regulates OVATE and auxin responses to modulate tomato gynoecium patterning and fruit morphology. bioRxiv. 2022. https://doi.org/10.1101/2022.03.15.484181.

[49] de Jong M, Mariani C, Vriezen WH . The role of auxin and gibberellin in tomato fruit set. J Exp Bot. 2009; 60: 1523-32.

[50] Hendelman A, Buxdorf K, Stav R et al. Inhibition of lamina outgrowth following Solanum lycopersicum AUXIN RESPONSE FACTOR 10 (SlARF10) derepression. Plant Mol Biol. 2012; 78: 561-76.

[51] Ren Z, Liu R, Gu W et al. The Solanum lycopersicum auxin response factor SlARF2 participates in regulating lateral root formation and flower organ senescence. Plant Sci. 2017; 256: 103-11.

[52] Zhao P, Wang F, Deng Y et al. Sly-miR159 regulates fruit morphology by modulating GA biosynthesis in tomato. Plant Biotechnol J. 2021; 20: 833-45.

[53] Chen S, Wang XJ, Tan GF et al. Gibberellin and the plant growth retardant paclobutrazol altered fruit shape and ripening in tomato. Protoplasma. 2020; 257: 853-61.

[54] Ohnishi T, Nomura T, Watanabe B et al. Tomato cytochrome P450 CYP734A7 functions in brassinosteroid catabolism. Phytochemistry. 2006; 67: 1895-906.

[55] Yu T, Ai G, Xie Q et al. Regulation of tomato fruit elongation by transcription factor BZR1.7 through promotion of SUN gene expression. Hortic Res. 2022; 9: uhac121.

[56] Zhou S, Hu Z, Li F et al. Overexpression of SlOFP20 affects floral organ and pollen development. Hortic Res. 2019; 6: 125.

[57] Guo X, Zhang Y, Tu Y et al. Overexpression of an EIN3-binding F-box protein2-like gene caused elongated fruit shape and delayed fruit development and ripening in tomato. Plant Sci. 2018; 272: 131-41.

[58] Guo H, Ecker JR . The ethylene signaling pathway: new insights. Curr Opin Plant Biol. 2004; 7: 40-9.

[59] Potuschak T, Lechner E, Parmentier Y et al. EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell. 2003; 115: 679-89.

[60] True JH, Shaw SL . Exogenous auxin induces transverse microtubule arrays through TRANSPORT INHIBITOR RESPONSE1/AUXIN SIGNALING F-BOX receptors. Plant Physiol. 2020; 182: 892-907.

[61] Wang Y, Ji Y, Fu Y et al. Ethylene-induced microtubule reorientation is essential for fast inhibition of root elongation in Arabidopsis. J Integr Plant Biol. 2018; 60: 864-77.

[62] Eng RC, Halat LS, Livingston SJ et al. The ARM domain of ARMADILLO-REPEAT KINESIN 1 is not required for microtubule catastrophe but can negatively regulate NIMA-RELATED KINASE 6 in Arabidopsis thaliana. Plant Cell Physiol. 2017; 58: 1350-63.

[63] Pnueli L, Gutfinger T, Hareven D et al. Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering. Plant Cell. 2001; 13: 2687-702.

[64] Soyk S, Lemmon ZH, Oved M et al. Bypassing negative epistasis on yield in tomato imposed by a domestication gene. Cell. 2017; 169: 1142-1155.e12.

[65] Yin S, Ao Q, Qiu T et al. Tomato SlYTH1 encoding a putative RNA m6A reader affects plant growth and fruit shape. Plant Sci. 2022; 323: 111417.

[66] Zheng Q, Takei-Hoshi R, Okumura H et al. Genome editing of SlMYB3R3, a cell cycle transcription factor gene of tomato, induces elongated fruit shape. J Exp Bot. 2022; 73: 7312-25.

[67] Che G, Zhang X . Molecular basis of cucumber fruit domestication. Curr Opin Plant Biol. 2019; 47: 38-46.

[68] Pan Y, Qu S, Bo K et al. QTL mapping of domestication and diversifying selection related traits in round-fruited semi-wild Xishuangbanna cucumber (Cucumis sativus L. var. xishuangbananesis). Theor Appl Genet. 2017; 130: 1531-48.

[69] Wei QZ, Fu WY, Wang YZ et al. Rapid identification of fruit length loci in cucumber (Cucumis sativus L.) using next-generation sequencing (NGS)-based QTL analysis. Sci Rep. 2016; 6: 27496.

[70] Weng Y, Colle M, Wang Y et al. QTL mapping in multiple populations and development stages reveals dynamic quantitative trait loci for fruit size in cucumbers of different market classes. Theor Appl Genet. 2015; 128: 1747-63.

[71] Pan Y, Liang X, Gao M et al. Round fruit shape in WI7239 cucumber is controlled by two interacting quantitative trait loci with one putatively encoding a tomato SUN homolog. Theor Appl Genet. 2017; 130: 573-86.

[72] Li H, Han J, Chen L et al. Ectopic expression of CsSUN in tomato results in elongated fruit shape via regulation of longitudinal cell division. Int J Mol Sci. 2022; 23: 9973.

[73] Xie Y, Liu X, Sun C et al. CsTRM5 regulates fruit shape via mediating cell division direction and cell expansion in cucumber. Hortic Res. 2023; 10: uhad007.

[74] Han L, Song X, Wang Z et al. Genome-wide analysis of OVATE family proteins in cucumber (Cucumis sativus L.). J Integr Agric. 2022; 21: 1321-31.

[75] Wang S, Lu G, Hou Z et al. Members of the tomato FRUITFULL MADS-box family regulate style abscission and fruit ripening. J Exp Bot. 2014; 65: 3005-14.

[76] Zhao J, Jiang L, Che G et al. A functional allele of CsFUL1 regulates fruit length through repressing CsSUP and inhibiting auxin transport in cucumber. Plant Cell. 2019; 31: 1289-307.

[77] Castaneda L, Gimenez E, Pineda B et al. Tomato CRABS CLAW paralogues interact with chromatin remodelling factors to mediate carpel development and floral determinacy. New Phytol. 2022; 234: 1059-74.

[78] Bowman JL, Smyth DR . CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development. 1999; 126: 2387-96.

[79] Che G, Pan Y, Liu X et al. Natural variation in CRABS CLAW contributes to fruit length divergence in cucumber. Plant Cell. 2022; 35: 738-55.

[80] Yang T, He Y, Niu S et al. A YABBY gene CRABS CLAW a (CRCa) negatively regulates flower and fruit sizes in tomato. Plant Sci. 2022; 320: 111285.

[81] Xin T, Zhang Z, Li S et al. Genetic regulation of ethylene dosage for cucumber fruit elongation. Plant Cell. 2019; 31: 1063-76.

[82] Zhang Z, Wang B, Wang S et al. Genome-wide target mapping shows Histone Deacetylase Complex1 regulates cell proliferation in cucumber fruit. Plant Physiol. 2020; 182: 167-84.

[83] Wang H, Sun J, Yang F et al. CsKTN1 for a katanin p60 subunit is associated with the regulation of fruit elongation in cucumber (Cucumis sativus L.). Theor Appl Genet. 2021; 134: 2429-41.

[84] Li Y, Deng M, Liu H et al. ABNORMAL SHOOT 6 interacts with KATANIN 1 and SHADE AVOIDANCE 4 to promote cortical microtubule severing and ordering in Arabidopsis. J Integr Plant Biol. 2021; 63: 646-61.

[85] Li D, Sheng Y, Niu H et al. Gene interactions regulating sex determination in cucurbits. Front Plant Sci. 2019; 10: 1231.

[86] Wittwer S, Hillyer I . Chemical induction of male sterility in cucurbits. Science. 1954; 120: 893-4.

[87] Boualem A, Berthet S, Devani RS et al. Ethylene plays a dual role in sex determination and fruit shape in cucurbits. Curr Biol. 2022; 32: 2390-2401.e4.

[88] Byers R, Baker L, Sell H et al. Ethylene: a natural regulator of sex expression of Cucumis melo L. Proc Natl Acad Sci USA. 1972; 69: 717-20.

[89] Li Z, Huang S, Liu S et al. Molecular isolation of the M gene suggests that a conserved-residue conversion induces the formation of bisexual flowers in cucumber plants. Genetics. 2009; 182: 1381-5.

[90] Switzenberg JA, Beaudry RM, Grumet R . Effect of CRC::etr1-1 transgene expression on ethylene production, sex expression, fruit set and fruit ripening in transgenic melon (Cucumis melo L.). Transgenic Res. 2015; 24: 497-507.

[91] Xu X, Wei C, Liu Q et al. The major-effect quantitative trait locus Fnl7.1 encodes a late embryogenesis abundant protein associated with fruit neck length in cucumber. Plant Biotechnol J. 2020; 18: 1598-609.

[92] Wang Y, Bo K, Gu X et al. Molecularly tagged genes and quantitative trait loci in cucumber with recommendations for QTL nomenclature. Hortic Res. 2020; 7: 3.

[93] Wang Z, Zhou Z, Wang L et al. The CsHEC1-CsOVATE module contributes to fruit neck length variation via modulating auxin biosynthesis in cucumber. Proc Natl Acad Sci USA. 2022; 119: e2209717119.

[94] Zhou H, Ma R, Gao L et al. A 1.7-Mb chromosomal inversion downstream of a PpOFP1 gene is responsible for flat fruit shape in peach. Plant Biotechnol J. 2021; 19: 192-205.

[95] Dirlewanger E, Pronier V, Parvery C et al. Genetic linkage map of peach [Prunus persica (L.) Batsch] using morphological and molecular markers. Theor Appl Genet. 1998; 97: 888-95.

[96] Dirlewanger E, Moing A, Rothan C et al. Mapping QTLs controlling fruit quality in peach (Prunus persica (L.) Batsch). Theor Appl Genet. 1999; 98: 18-31.

[97] Guan J, Xu Y, Yu Y et al. Genome structure variation analyses of peach reveal population dynamics and a 1.67 Mb causal inversion for fruit shape. Genome Biol. 2021; 22: 13.

[98] Guo J, Cao K, Deng C et al. An integrated peach genome structural variation map uncovers genes associated with fruit traits. Genome Biol. 2020; 21: 258.

[99] Liu D, Sun W, Yuan Y et al. Phylogenetic analyses provide the first insights into the evolution of OVATE family proteins in land plants. Ann Bot. 2014; 113: 1219-33.

[100] Wang S, Chang Y, Guo J et al. Arabidopsis ovate family proteins, a novel transcriptional repressor family, control multiple aspects of plant growth and development. PLoS One. 2011; 6: e23896.

[101] Zhang X, Wu J, Yu Q et al. AtOFPs regulate cell elongation by modulating microtubule orientation via direct interaction with TONNEAU2. Plant Sci. 2020; 292: 110405.

[102] Wang S, Chang Y, Guo J et al. Arabidopsis Ovate Family Protein 1 is a transcriptional repressor that suppresses cell elongation. Plant J. 2007; 50: 858-72.

[103] Wang X, Wang W, Wang J et al. Class III OFPs function in the ER signaling pathway to regulate plant growth and development in Arabidopsis. J Plant Interact. 2018; 14: 45-53.

[104] Drevensek S, Goussot M, Duroc Y et al. The Arabidopsis TRM1-TON1 interaction reveals a recruitment network common to plant cortical microtubule arrays and eukaryotic centrosomes. Plant Cell. 2012; 24: 178-91.

[105] Lee YK, Kim G-T, Kim I-J et al. LONGIFOLIA1 and LONGIFOLIA2, two homologous genes, regulate longitudinal cell elongation in Arabidopsis. Development. 2006; 133: 4305-14.

[106] Spinner L, Gadeyne A, Belcram K et al. A protein phosphatase 2A complex spatially controls plant cell division. Nat Commun. 2013; 4: 1863.

[107] Li N, Xu R, Li Y . Molecular networks of seed size control in plants. Annu Rev Plant Biol. 2019; 70: 435-63.

[108] Yue ZL, Liu N, Deng ZP et al. The receptor kinase OsWAK11 monitors cell wall pectin changes to fine-tune brassinosteroid signaling and regulate cell elongation in rice. Curr Biol. 2022; 32: 2454-2466.e7.

[109] Yuan H, Xu Z, Chen W et al. OsBSK2, a putative brassinosteroid-signaling kinase, positively controls grain size in rice. J Exp Bot. 2022; 73: 5529-42.

[110] Nolan TM, Vukasinovic N, Liu D et al. Brassinosteroids: multidimensional regulators of plant growth, development, and stress responses. Plant Cell. 2020; 32: 295-318.

[111] Zhao DS, Li QF, Zhang CQ et al. GS9 acts as a transcriptional activator to regulate rice grain shape and appearance quality. Nat Commun. 2018; 9: 1240.

[112] Tong H, Liu L, Jin Y et al. DWARF AND LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice. Plant Cell. 2012; 24: 2562-77.

[113] Yang C, Shen W, He Y et al. OVATE family protein 8 positively mediates brassinosteroid signaling through interacting with the GSK3-like kinase in rice. PLoS Genet. 2016; 12: e1006118.

[114] Xiao Y, Liu D, Zhang G et al. Brassinosteroids regulate OFP1, a DLT interacting protein, to modulate plant architecture and grain morphology in rice. Front Plant Sci. 2017; 8: 1698.

[115] Xiao Y, Zhang G, Liu D et al. GSK2 stabilizes OFP3 to suppress brassinosteroid responses in rice. Plant J. 2020; 102: 1187-201.

[116] Gruszka D. Exploring the brassinosteroid signaling in monocots reveals novel components of the pathway and implications for plant breeding. Int J Mol Sci. 2020; 21: 354.

[117] Yang C, Ma Y, He Y et al. OsOFP19 modulates plant architecture by integrating the cell division pattern and brassinosteroid signaling. Plant J. 2018; 93: 489-501.

[118] Tsuda K, Kurata N, Ohyanagi H et al. Genome-wide study of KNOX regulatory network reveals brassinosteroid catabolic genes important for shoot meristem function in rice. Plant Cell. 2014; 26: 3488-500.

[119] Chen H, Yu H, Jiang W et al. Overexpression of ovate family protein 22 confers multiple morphological changes and represses gibberellin and brassinosteroid signalings in transgenic rice. Plant Sci. 2021; 304: 110734.

[120] Schmitz AJ, Begcy K, Sarath G et al. Rice ovate family protein 2 (OFP2) alters hormonal homeostasis and vasculature development. Plant Sci. 2015; 241: 177-88.

[121] Ma Y, Yang C, He Y et al. Rice OVATE family protein 6 regulates plant development and confers resistance to drought and cold stresses. J Exp Bot. 2017; 68: 4885-98.

[122] Gallego-Bartolome J, Minguet EG, Grau-Enguix F et al. Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc Natl Acad Sci USA. 2012; 109: 13446-51.

[123] Stewart Lilley JL, Gan Y, Graham IA et al. The effects of DELLAs on growth change with developmental stage and brassinosteroid levels. Plant J. 2013; 76: 165-73.

[124] Tong H, Xiao Y, Liu D et al. Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell. 2014; 26: 4376-93.

[125] Li Q-F, Wang C, Jiang L et al. An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci Signal. 2012; 5: ra72.

[126] Wang Y, Xiong G, Hu J et al. Copy number variation at the GL7 locus contributes to grain size diversity in rice. Nat Genet. 2015; 47: 944-8.

[127] Wang S, Li S, Liu Q et al. The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet. 2015; 47: 949-54.

[128] Zhou Y, Miao J, Gu H et al. Natural variations in SLG7 regulate grain shape in rice. Genetics. 2015; 201: 1591-9.

[129] Wang S, Wu K, Yuan Q et al. Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet. 2012; 44: 950-4.

[130] Xing S, Salinas M, Garcia-Molina A et al. SPL8 and miR156-targeted SPL genes redundantly regulate Arabidopsis gynoecium differential patterning. Plant J. 2013; 75: 566-77.

[131] Kumari P, Dahiya P, Livanos P et al. IQ67 DOMAIN proteins facilitate preprophase band formation and division-plane orientation. Nat Plants. 2021; 7: 739-47.

[132] Bürstenbinder K, Möller B, Plötner R et al. The IQD family of calmodulin-binding proteins links calcium signaling to microtubules, membrane subdomains, and the nucleus. Plant Physiol. 2017; 173: 1692-708.

[133] Abel S, Savchenko T, Levy M . Genome-wide comparative analysis of the IQD gene families in Arabidopsis thaliana and Oryza sativa. BMC Evol Biol. 2005; 5: 72.

[134] Levy M, Wang Q, Kaspi R et al. Arabidopsis IQD1, a novel calmodulin-binding nuclear protein, stimulates glucosinolate accumulation and plant defense. Plant J. 2005; 43: 79-96.

[135] Burstenbinder K, Savchenko T, Muller J et al. Arabidopsis calmodulin-binding protein IQ67-domain 1 localizes to microtubules and interacts with kinesin light chain-related protein-1. J Biol Chem. 2013; 288: 1871-82.

[136] Liang H, Zhang Y, Martinez P et al. The microtubule-associated protein IQ67 DOMAIN5 modulates microtubule dynamics and pavement cell shape. Plant Physiol. 2018; 177: 1555-68.

[137] Mitra D, Klemm S, Kumari P et al. Microtubule-associated protein IQ67 DOMAIN5 regulates morphogenesis of leaf pavement cells in Arabidopsis thaliana. J Exp Bot. 2019; 70: 529-43.

[138] Vaddepalli P, de Zeeuw T, Strauss S et al. Auxin-dependent control of cytoskeleton and cell shape regulates division orientation in the Arabidopsis embryo. Curr Biol. 2021; 31: 4946-4955.e4.

[139] Duan P, Xu J, Zeng D et al. Natural variation in the promoter of GSE5 contributes to grain size diversity in rice. Mol Plant. 2017; 10: 685-94.

[140] Liu J, Chen J, Zheng X et al. GW5 acts in the brassinosteroid signalling pathway to regulate grain width and weight in rice. Nat Plants. 2017; 3: 17043.

[141] Möller BK, Hove CA, Xiang D et al. Auxin response cell-autonomously controls ground tissue initiation in the early Arabidopsis embryo. Proc Natl Acad Sci USA. 2017; 114: E2533-9.

[142] Burstenbinder K, Mitra D, Quegwer J . Functions of IQD proteins as hubs in cellular calcium and auxin signaling: a toolbox for shape formation and tissue-specification in plants? Plant Signal Behav. 2017; 12: e1331198.

[143] Monshausen GB, Miller ND, Murphy AS et al. Dynamics of auxin-dependent Ca2+ and pH signaling in root growth revealed by integrating high-resolution imaging with automated computer vision-based analysis. Plant J. 2011; 65: 309-18.

[144] Yang B, Wendrich JR, Rybel BD et al. OsIQD14 regulates rice grain shape through modulating the microtubule cytoskeleton. bioRxiv. 2018.

[145] Schaefer E, Belcram K, Uyttewaal M et al. The preprophase band of microtubules controls the robustness of division orientation in plants. Science. 2017; 356: 186-9.

[146] Stöckle D, Herrmann A, Lipka E et al. Putative RopGAPs impact division plane selection and interact with kinesin-12 POK1. Nat Plants. 2016; 2: 16120.

[147] Azimzadeh J, Nacry P, Christodoulidou A et al. Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. Plant Cell. 2008; 20: 2146-59.

[148] Buschmann H, Fabri CO, Hauptmann M et al. Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr Biol. 2004; 14: 1515-21.