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Soybean GmRSM1 promotes apical hook disappearance by regulating PIN gene expression

FU Jia-Qi1,2, LI Shi-Kuan1,2,TAN Meng-Hui1,2,LUO Fang3,ZHANG Chuan-Ling3,LIU Ling-Yue3,LU Qian1,*,GU Yong-Zhe1,2,*   

  1. 1College of Life Sciences and Technology, Harbin Normal University, Harbin 150025, Heilongjiang, China; 2Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China; 3Arong Banner Agricultural Development Center, Arong Banner 162750, Inner Mongolia, China
  • Received:2024-02-05 Revised:2024-06-20 Accepted:2024-06-20 Published:2024-07-10
  • Supported by:
    This study was supported by the National Natural Science Foundation of China (32372190).

Abstract:

The apical hook is a transient structure found in etiolated dicot seedlings, and while the current model for the apical hook in Arabidopsis thaliana is relatively well-established, there is limited research on soybean. In this study, the pBAR-GmRSM1 overexpression vector was constructed, and three homozygous lines each of Arabidopsis thaliana (OE-GmRSM1#64, #69, and #70) and soybean (OE-GmRSM1#103, #78, and #95) were generated through genetic transformation and positive plant selection. The expression levels of the transgenic lines were significantly higher compared to the wild type. Both Arabidopsis thaliana and soybean cultures were grown in darkness, and the apical hooks in the overexpressed transformants disappeared or exhibited faster disappearance compared to the wild type. Scanning electron microscopy observations of cell length in the apical hook of Arabidopsis thaliana wild-type and transformant plants revealed that the inner hook cells were shorter than the outer hook cells during the hook maintenance stage, while the cell lengths were the same on both sides in the transformant plants. The inner and outer sides of the soybean apical hook were separated, and the expression of the PIN gene in the wild type and three overexpressed transformants of soybean was analyzed. The results demonstrated that the expression levels of the PIN1e, PIN3d, and PIN6a genes were significantly higher in the apical hook after cotyledon unfolding, and during the hook maintenance stage, these three genes exhibited significantly higher expression levels in the transformants compared to the wild type, but there was no significant difference in expression levels after unfolding. Transient expression in tobacco confirmed the localization of the GmRSM1 protein in the nucleus and cell membrane. Thus, the apical hook formation is attributed to differential cell elongation between the inner and outer sides of the hook, leading to hypocotyl curvature. GmRSM1 regulates the expression of auxin transporters PIN1e, PIN3d, and PIN6a, thereby shortening the duration of hook maintenance and unfolding. These genes are positively regulated by GmRSM1 during the hook stage, and the study confirmed the regulatory effect of this gene on auxin. Overall, this study verified the role of the GmRSM1 gene in the disappearance of the apical hook phenotype and further elucidated the gene pathway involved in apical curvature, laying a foundation for future research.

Key words: apical hook, soybean, Arabidopsis, PIN family, auxin

[1] Veloccia A, Fattorini L, Della Rovere F, Sofo A, D' Angeli S, Betti C, Falasca G, Altamura M M. Ethylene and auxin interaction in the control of adventitious rooting in Arabidopsis thaliana. J Exp Bot, 2016, 67: 6445–6458.

[2] Shen X, Li Y, Pan Y, Zhong S. Activation of HLS1 by mechanical stress via ethylene-stabilized EIN3 is crucial for seedling soil emergence. Front Plant Sci, 2016, 7: 1571.

[3] Peng Y, Zhang D, Qiu Y, Xiao Z, Ji Y, Li W, Xia Y, Wang Y, Guo H. Growth asymmetry precedes differential auxin response during apical hook initiation in Arabidopsis. J Integr Plant Biol, 2022, 64: 5–22.

[4] Shi H, Liu R, Xue C, Shen X, Wei N, Deng X W, Zhong S. Seedlings transduce the depth and mechanical pressure of covering soil using COP1 and ethylene to regulate EBF1/EBF2 for soil emergence. Curr Biol, 2016, 26: 139–149.

[5] Silk W, Erickson R. Kinematics of hypocotyl curvature. Am J Bot, 1978, 65: 310–319.

[6] Weijers D, Nemhauser J, Yang Z. Auxin: small molecule, big impact. J Exp Bot, 2018, 69: 133–136.

[7] Schwark A, Schierle J. Interaction of ethylene and auxin in the regulation of hook growth II. The role for ethylene in different growing regions of the hypocotyl hook of phaseolus vulgaris. J. Plant Physiol, 1993, 140: 562–570.

[8] Žádníková P, Wabnik K, Abuzeineh A, Gallemi M, Van Der Straeten D, Smith RS, Inzé D, Friml J, Prusinkiewicz P, Benková E. A model of differential growth-guided apical hook formation in plants. Plant Cell, 2016, 28: 2464–2477.

[9] Hamaguchi A, Yamashino T, Koizumi N, Kiba T, Kojima M, Sakakibara H, Mizuno T. A small subfamily of Arabidopsis RADIALIS-LIKE SANT/MYB genes: a link to HOOKLESS1-mediated signal transduction during early morphogenesis. Biosci Biotechnol Biochem, 2008, 72: 2687–96.

[10] Béziat C, Kleine-Vehn J. The road to auxin-dependent growth repression and promotion in apical hooks. Curr Biol, 2018, 28: R519–R525.

[11] Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazímalová E. The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol, 2009, 10: 249.

[12] Zádníková P, Petrásek J, Marhavy P, Raz V, Vandenbussche F, Ding Z, Schwarzerová K, Morita M T, Tasaka M, Hejátko J, Van Der Straeten D, Friml J, Benková E. Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development, 2010, 137: 607–617.

[13] Wang Y, Chai C, Valliyodan B, Maupin C, Annen B, Nguyen H T. Genome-wide analysis and expression profiling of the PIN auxin transporter gene family in soybean (Glycine max). BMC Genomics, 2015, 16: 951.

[14] Clough S J, Bent A F. Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant J, 1998, 16: 735–743.

[15] Wang Y, Li Z, Chen X, Gu Y, Zhang L, Qiu L. An efficient soybean transformation protocol for use with elite lines. Plant Cell Tissue Organ Cult., 2022, 151: 457–466.

[16] Cheng G, Dong M, Xu Q, Peng L, Yang Z, Wei T, Xu J. Dissecting the molecular mechanism of the subcellular localization and cell-to-cell movement of the Sugarcane mosaic virus P3N-PIPO. Sci Rep, 2017, 7: 9868.

[17] Wu Q, Li Y, Lyu M, Luo Y, Shi H, Zhong S. Touch-induced seedling morphological changes are determined by ethylene-regulated pectin degradation. Sci Adv, 2020, 6: eabc9294.

[18] Wang Y, Guo H. On hormonal regulation of the dynamic apical hook development. New Phytol, 2019, 222: 1230–1234.

[19] Li H, Johnson P, Stepanova A, Alonso J M, Ecker J R. Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev Cell, 2004, 7: 193–204.

[20] Chai C, Wang Y, Valliyodan B, Nguyen H T. Comprehensive analysis of the soybean (Glycine max) GmLAX auxin transporter gene family. Front Plant Sci, 2016, 7: 282.

[21]Baxter C E, Costa M M, Coen E S. Diversification and co-option of RAD-like genes in the evolution of floral asymmetry. Plant J, 2007, 52: 105–113.

[22] Costa M M, Fox S, Hanna A I, Baxter C, Coen E. Evolution of regulatory interactions controlling floral asymmetry. Development, 2005, 132: 5093–5101.

[23] Corley S B, Carpenter R, Copsey L, Coen E. Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. Proc Natl Acad Sci USA, 2005, 102: 5068–5073. 

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