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Regulation of Suberin Biosynthesis and Casparian Strip Development In bioRxiv preprint doi: https://doi.org/10.1101/2021.06.02.446769; this version posted June 3, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Regulation of suberin biosynthesis and 2 Casparian strip development in the root 3 endodermis by two plant auxins 4 Short title: Auxin regulates suberin and the casparian strip. 5 Cook, Sam Davida, 1, Kimura, Seisukeb,c, Wu, Qi d, Franke, Rochus Bennie, Kamiya, Takehirod, 6 Kasahara, Hiroyukif, 1 7 a Institute of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Japan 183- 8 0057, b Faculty of Life Sciences, Kyoto Sangyo University, Japan 603-8555, c Center for Plant 9 Sciences, Kyoto Sangyo University, Kyoto, Japan, d Graduate School of Agricultural and Life 10 Sciences, University of Tokyo, Tokyo, Japan 113-8654, e Institute of Cellular and Molecular 11 Botany, University of Bonn, Bonn, Germany 53115, f Institute of Global Innovation Research, 12 Tokyo University of Agriculture and Technology, Fuchu, Japan 183-0057 13 1Corresponding authors: Sam Cookg, Hiroyuki Kasahara, Tokyo University of Agriculture and 14 Technology, 3-5-8 Saiwai-cho, Fuchu-shi, Tokyo 183-0054, Japan, g Current address: Department 15 of Chemistry, Umeå University, Umeå, Sweden 90187. 16 Tel: +81-42-367-5796 17 Email: [email protected], [email protected] 18 One sentence summary: Phenylacetic acid, a plant auxin, plays a unique role in the regulation of 19 the root endodermal barrier that is distinct from the classical auxin, indole-3-acetic acid. 20 Author contributions: SDC, HK and TK planned and designed the research, SDC, SK, WQ and RBF 21 performed experiments, SDC, SK, WQ, RBF and TK analyzed data, SDC wrote the manuscript. 22 Funding information: This work was supported by Japan Society for the Promotion of Science 23 KAKENHI [18F18708 to S.D.C.], [20K21419 to H.K.] and [17H03782 to T.K.]. This work is partially 24 supported by the MEXT Supported Program for the Strategic Research Foundation at Private 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.02.446769; this version posted June 3, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 25 Universities from the Ministry of Education, Culture, Sports, Science & Technology of Japan, 26 [Grant No. S1511023 to S.K.] 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.02.446769; this version posted June 3, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 27 Abstract 28 The biological function of the auxin phenylacetic acid (PAA) is not well characterized in plants. 29 Although some aspects of its biology; transport, signaling and metabolism have recently been 30 described. Previous work on this phytohormone has suggested that PAA behaves in an identical 31 manner to IAA (indole-3-acetic acid) in promoting plant growth, yet plants require greater 32 concentrations of PAA to elicit the same physiological responses. Here we show that normalized 33 PAA treatment results in the differential expression of a unique list of genes, suggesting that 34 plants can respond differently to the two auxins. This is further explored in endodermal barrier 35 regulation where the two auxins invoke striking differences in the deposition patterns of 36 suberin. We further show that auxin acts antagonistically on Casparian strip (CS) formation as it 37 can circumvent the CS transcriptional machinery to repress CS related genes. Additionally, 38 altered suberin biosynthesis reduces endogenous levels of PAA and CS deficiency represses the 39 biosynthesis of IAA and the levels of both auxins. These findings implicate auxin as a regulator of 40 endodermal barrier formation and highlight a novel role for PAA in root development and 41 differentiation. 42 Keywords: Auxin, Casparian Strip (CS), Endodermis, Indole-3-acetic acid (IAA), Phenylacetic acid 43 (PAA), Root Development, Suberin. 44 45 Introduction 46 The auxin phenylacetic acid (PAA) has a long history as a phytohormone, but only little is known 47 about its biological function in plants (Cook, 2019). PAA shares several similarities with the well- 48 studied indole-3-acetic acid (IAA) including its perception via the TIR1/AFB receptor complex 49 (Shimizu-Mitao and Kakimoto, 2014). PAA typically has reduced potency when compared with 50 IAA, although endogenous concentrations of PAA are often higher (Sugawara et al., 2015). PAA 51 also possesses unique transport characteristics and is relatively immobile in plants due to its 52 inability to be actively transported (Morris and Johnson, 1987). This auxin is most active in plant 53 roots where exogenous treatment stimulates significant emergence of lateral roots (Sugawara 54 et al., 2015). 55 Roots themselves produce a hydrophobic biopolymer that is comprised of numerous aliphatic 56 and aromatic monomers, known as suberin (Geldner, 2013). In Arabidopsis roots, suberin is 57 located in the endodermis where it functions as a transmembrane barrier in conjunction with 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.02.446769; this version posted June 3, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 58 the Casparian strip (Barberon, 2017). Suberin is deposited as a continuous lamella which is 59 located on the interior of the cell wall, external to the plasma membrane (Barberon et al., 2016). 60 This barrier works to prevent pathogen infection (Holbein et al., 2019), to regulate nutrient 61 uptake (Barberon, 2017) and to limit radial oxygen loss (Kotula et al., 2009; Ranathunge and 62 Schreiber, 2011). While still incomplete, the biosynthesis of suberin is well characterized in 63 Arabidopsis and is described elsewhere (Vishwanath et al., 2015). 64 Plant hormones have previously been shown to influence the deposition of suberin, where the 65 antagonistic action of abscisic acid (ABA) and ethylene control the suberization of root tissue 66 (Barberon et al., 2016). In general, ethylene reduces suberization, while ABA promotes ectopic 67 suberization in Arabidopsis roots (Barberon et al., 2016). Currently, the downstream 68 mechanisms by which ABA and ethylene act are not understood (Barberon, 2017). In addition to 69 these two hormones, it has also been reported that IAA treatment can upregulate expression of 70 the putative suberin monomer transporters ABCG6 and ABCG20 (Yadav et al., 2014) and 71 treatment with the synthetic auxin NAA (1-Naphthaleneacetic acid) results in altered expression 72 of the GDSL-lipases, associated with the (dis)-assembly of the suberin polymer (Ursache et al., 73 2020). However, the effect of endogenous auxin on suberin biology has not been explored in 74 much detail. 75 The Casparian strip (CS) is a cell wall modification whereby a lignin-polymer is deposited in the 76 apoplastic space between endodermal cells in the differentiation zone of growing roots 77 (Geldner, 2013). The deposition of CS results in a sheath that encloses root vascular bundles and 78 fuses adjacent cell walls, creating an apoplastic barrier (Enstone et al., 2002). There is no current 79 description of phytohormonal control over CS development aside from the recently described 80 Casparian Strip Integrity Factor (CIF) peptide hormones, which act as a diffusible signal 81 indicating the status of the CS (Matsubayashi et al., 2017). The CIFs are perceived by the 82 Schengen kinases (SGN1 and SGN3), which are located on the endodermal plasma membrane 83 interior to the CS (Doblas et al., 2017). While currently uncharacterized, the activated kinases 84 communicate CS deficiency, likely inducing MYB36, a regulator of Casparian strip development 85 (Kamiya et al., 2015). 86 Here we demonstrate that the role auxins play in barrier formation is far more complex than 87 previously described (Yadav et al., 2014; Ursache et al., 2020). We have shown that auxin 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.02.446769; this version posted June 3, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 88 promotes suberin biosynthesis at both high and low concentrations and that PAA treatment 89 results in a completely different suberin deposition pattern than IAA, suggesting that the two 90 auxins likely work together to promote root suberization at different developmental stages. We 91 also show that both IAA and PAA treatment has a negative effect on Casparian strip regulation, 92 particularly on the CASP (CASPARIAN STRIP MEMBRANE DOMAIN PROTEINS) and ESB 93 (ENHANCED SUBERIN 1) family genes, and on PER64, which are essential for normal CS 94 deposition. However, auxin does not appear to affect CS transcription factors. In addition to 95 influencing these root developmental processes, we have further shown that there is substantial 96 feedback regulation on IAA biosynthesis by CS state and thus we propose a model by which 97 auxin functions in the maintenance of the CS and of its initial establishment. Overall, these 98 findings demonstrate that auxin is an integral regulator of endodermal barrier production.
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