A perspective on the molecular mechanism in the control of organ internal (IN) asymmetry during petal development

Abstract

Floral zygomorphy (monosymmetry) is a key innovation in flowering plants and is related to the coevolution of plants and their animal pollinators. The molecular basis underlying floral zygomorphy has been analysed, and two regulatory pathways have been identified: one determines the dorsoventral (DV) asymmetry along the floral plan, and the other controls organ internal (IN) asymmetry during petal development. While strides have been made to understand the molecular mechanism controlling DV asymmetry, which mainly involves an interplay between TCP and MYB transcription factors, the molecular pathway regulating IN asymmetry remains largely unknown. In this review, we discuss what is known about regulators and the molecular pathway regulating IN asymmetry. Our analysis revealed that the regulation of IN asymmetry occurs at the cellular, tissue, and organ genesis levels during petal development and that the regulatory mechanism is likely integrated into different developmental paths, such as floral and root nodule development. Although the molecular regulation of IN asymmetry is not be a linear path, a key hub for the regulatory network could be vascular patterning during petal organogenesis.

References

[1] Bahadur B, Krishnamurthy KV, Ghose M et al. Asymmetry in Plants: Biology of Handedness. Boca Raton, Florida, USA: CRC Press; 2019.

[2] Giurfa M, Dafni A, Neal PR . Floral symmetry and its role in plant-pollinator systems. Int J Plant Sci. 1999; 160: S41-50.

[3] Jesson LK, Barrett SC . Solving the puzzle of mirror-image flowers. Nature. 2002; 417: 707.

[4] Kalisz S, Ree RH, Sargent D . Linking floral symmetry genes to breeding system evolution. Trends Plant Sci. 2006; 11: 568-73.

[5] Dworaczek E, Claßen-Bockhoff R . ‘False resupination’ in the flower-pairs of Thalia (Marantaceae). Flora. 2016; 221: 65-74.

[6] Endress PK . Symmetry in flowers: diversity and evolution. Int J Plant Sci. 1999; 160: S3-23.

[7] Luo D, Carpenter R, Vincent C et al. Origin of floral asymmetry in antirrhinum. Nature. 1996; 383: 794-9.

[8] Luo D, Carpenter R, Copsey L et al. Control of organ asymmetry in flowers of antirrhinum. Cell. 1999; 99: 367-76.

[9] Corley SB, Carpenter R, Copsey L et al. Floral asymmetry involves an interplay between TCP and MYB transcription factors in antirrhinum. Proc Natl Acad Sci U S A. 2005; 102: 5068-73.

[10] Raimundo J, Sobral R, Bailey P et al. A subcellular tug of war involving three MYB-like proteins underlies a molecular antagonism in antirrhinum flower asymmetry. Plant J. 2013; 75: 527-38.

[11] Rolland-Lagan AG, Bangham JA, Coen E . Growth dynamics underlying petal shape and asymmetry. Nature. 2003; 422: 161-3.

[12] Hileman LC, Kramer EM, Baum DA . Differential regulation of symmetry genes and the evolution of floral morphologies. Proc Natl Acad Sci U S A. 2003; 100: 12814-9.

[13] Gaudin V, Lunness PA, Fobert PR et al. The expression of D-cyclin genes defines distinct developmental zones in snapdragon apical meristems and is locally regulated by the Cycloidea gene. Plant Physiol. 2000; 122: 1137-48.

[14] Wang Z, Luo Y, Li X et al. Genetic control of floral zygomorphy in pea (Pisum sativum L.). Proc Natl Acad Sci U S A. 2008; 105: 10414-9.

[15] Wang J, Wang Y, Luo D . LjCYC genes constitute floral dorsoventral asymmetry in Lotus japonicus. J Integr Plant Biol. 2010; 52: 959-70.

[16] Feng X, Zhao Z, Tian Z et al. Control of petal shape and floral zygomorphy in Lotus japonicus. Proc Natl Acad Sci U S A. 2006; 103: 4970-5.

[17] Li X, Zhuang LL, Ambrose M et al. Genetic analysis of ele mutants and comparative mapping of ele1 locus in the control of organ internal asymmetry in garden pea. J Integr Plant Biol. 2010; 52: 528-35.

[18] Li X, Liu W, Zhuang L et al. BIGGER ORGANS and ELEPHANT EAR-LIKE LEAF1 control organ size and floral organ internal asymmetry in pea. J Exp Bot. 2019; 70: 179-91.

[19] He L, Lei Y, Li X et al. SYMMETRIC PETALS 1 encodes an ALOG domain protein that controls floral organ internal asymmetry in pea (Pisum sativum L.). Int J Mol Sci. 2020; 21: 4060.

[20] Thakur JK, Agarwal P, Parida S et al. Sequence and expression analyses of KIX domain proteins suggest their importance in seed development and determination of seed size in rice, and genome stability in Arabidopsis. Mol Gen Genomics. 2013; 288: 329-46.

[21] Ge L, Yu J, Wang H et al. Increasing seed size and quality by manipulating BIG SEEDS1 in legume species. Proc Natl Acad Sci U S A. 2016; 113: 12414-9.

[22] White DW . PEAPOD regulates lamina size and curvature in Arabidopsis. Proc Natl Acad Sci U S A. 2006; 103: 13238-43.

[23] Gonzalez N, Pauwels L, Baekelandt A et al. A repressor protein complex regulates leaf growth in Arabidopsis. Plant Cell. 2015; 27: 2273-87.

[24] Zhuang LL, Ambrose M, Rameau C et al. LATHYROIDES, encoding a WUSCHEL-related Homeobox1 transcription factor, controls organ lateral growth, and regulates tendril and dorsal petal identities in garden pea (Pisum sativum L.). Mol Plant. 2012; 5: 1333-45.

[25] Couzigou JM, Zhukov V, Mondy S et al. NODULE ROOT and COCHLEATA maintain nodule development and are legume orthologs of Arabidopsis BLADE-ON-PETIOLE genes. Plant Cell. 2012; 24: 4498-510.

[26] Yaxley J . Leaf and flower development in pea (Pisum sativum L.): mutants cochleata and unifoliata. Ann Bot. 2001; 88: 225-34.

[27] Guo W, Zhang X, Peng Q et al. Love on wings, a Dof family protein regulates floral vasculature in Vigna radiata. BMC Plant Biol. 2019; 19: 495.

[28] Dengler N, Kang J . Vascular patterning and leaf shape. Curr Opin Plant Biol. 2001; 4: 50-6.

[29] Nelson T, Dengler N . Leaf vascular pattern formation. Plant Cell. 1997; 9: 1121-35.

[30] Petricka JJ, Clay NK, Nelson TM . Vein patterning screens and the defectively organized tributaries mutants in Arabidopsis thaliana. Plant J. 2008; 56: 251-63.

[31] Ruonala R, Ko D, Helariutta Y . Genetic networks in plant vascular development. Annu Rev Genet. 2017; 51: 335-59.

[32] De Rybel B, Adibi M, Breda AS et al. Plant development. Integration of growth and patterning during vascular tissue formation in Arabidopsis. Science. 2014; 345: 1255215.

[33] Mähönen AP, Bishopp A, Higuchi M et al. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science. 2006; 311: 94-8.

[34] Gälweiler L, Guan C, Müller A et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science. 1998; 282: 2226-30.

[35] Sieburth LE et al. SCARFACE encodes an ARF-GAP that is required for normal auxin efflux and vein patterning in Arabidopsis. Plant Cell. 2006; 18: 1396-411.

[36] Govindaraju P, Verna C, Zhu T et al. Vein patterning by tissue-specific auxin transport. Development. 2020; 147: dev187666.

[37] Scarpella E, Marcos D, Friml J et al. Control of leaf vascular patterning by polar auxin transport. Genes Dev. 2006; 20: 1015-27.

[38] Burian A, Raczyńska-Szajgin M, Pałubicki W . Shaping leaf vein pattern by auxin and mechanical feedback. J Exp Bot. 2021; 72: 964-7.

[39] Lavania D, Linh NM, Scarpella E . Of cells, strands, and networks: auxin and the patterned formation of the vascular system. Cold Spring Harb Perspect Biol. 2021; 13: a039958.

[40] Coen ES, Nugent JM . Evolution of flowers and inflorescences. Development. 1994; 1994: 107-16.

[41] Citerne H, Jabbour F, Nadot S et al. The evolution of floral symmetry. Adv Bot Res. 2010; 54: 85-137.

[42] Stebbins GL . Flowering Plants: Evolution above the Species Level. Massachusetts, USA: Harvard University Press; 1974.

[43] Li W, Zhou Y, Liu X et al. LEAFY controls auxin response pathways in floral primordium formation. Sci Signal. 2013; 6: ra23.

[44] Benková E, Michniewicz M, Sauer M et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 2003; 115: 591-602.

[45] Lönnig WE, Stüber K, Saedler H et al. Biodiversity and Dollo’s law: to what extent can the phenotypic differences between Misopates orontium and Antirrhinum majus be bridged by mutagenesis? Bioremediation, Biodiversity and Bioavailability. 2007; 1: 1-30.

[46] Sengupta A, Hileman LC . A CYC-RAD-DIV-DRIF interaction likely predates the origin of floral monosymmetry in Lamiales. EvoDevo. 2022; 13: 1-19.