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Cjb-2020-0012.Pdf Botany Reactive oxygen species are required for spore wall formation in Physcomitrella patens Journal: Botany Manuscript ID cjb-2020-0012.R1 Manuscript Type: Article Date Submitted by the 22-May-2020 Author: Complete List of Authors: Rabbi, Fazle; University of Regina, Chemistry and Biochemistry Renzaglia, Karen; Southern Illinois University Carbondale, Plant Biology Ashton, Neil; University of Regina, Chemistry and Biochemistry Suh, Dae-Yeon;Draft University of Regina, Chemistry and Biochemistry augmented osmolysis, exine, perine, oxidative cross-linking, Keyword: sporopollenin polymerization Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : https://mc06.manuscriptcentral.com/botany-pubs Page 1 of 32 Botany 1 Reactive oxygen species are required for spore wall formation in Physcomitrella patens 2 3 Fazle Rabbi, Karen S. Renzaglia, Neil W. Ashton, Dae-Yeon Suh 4 5 6 7 F. Rabbi ([email protected]), N.W. Ashton ([email protected]), and D.-Y. Suh 8 ([email protected]), Department of Chemistry and Biochemistry, University of Regina, Regina, 9 SK S4S 0A2, Canada 10 K.S. Renzaglia ([email protected]), Department of Plant Biology, Southern Illinois University, 11 Carbondale, IL 62901, USA Draft 12 13 14 15 Corresponding author: 16 Dae-Yeon Suh, Department of Chemistry and Biochemistry, University of Regina, Regina, SK 17 S4S 0A2, Canada. 18 E-mail: [email protected] 19 Tel: +1 306 585 4239 20 Fax: +1 306 337 2409 1 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 2 of 32 21 Abstract: 22 A robust spore wall was a key requirement of terrestrialization by early plants. Sporopollenin in 23 spore and pollen grain walls is thought to be polymerized and cross-linked to other 24 macromolecular components partly through oxidative processes involving H2O2. Therefore, we 25 investigated effects of scavengers of reactive oxygen species (ROS) on formation of spore walls 26 in the moss, Physcomitrella patens. Exposure of sporophytes, containing spores in the process of 27 forming walls, to ascorbate, dimethylthiourea or 4-hydroxy-TEMPO prevented normal wall 28 development in a dose, chemical and stage-dependent manner. Mature spores, exposed while 29 developing to a ROS scavenger, burst when mounted in water on a flat slide under a coverslip (a 30 phenomenon we named “augmented osmolysis” since they did not burst in phosphate-buffered 31 saline or in water on a depression slide).Draft Additionally, walls of exposed spores were more 32 susceptible to alkaline hydrolysis than those of control spores and some were characterized by 33 discontinuities in the exine, anomalies in perine spine structure, abnormal intine and aperture and 34 occasionally wall shedding. Our data support involvement of oxidative cross-linking in spore wall 35 development, including sporopollenin polymerization or deposition, as well as a role for ROS in 36 intine/aperture development. 37 38 Key words: augmented osmolysis, exine, perine, intine, oxidative cross-linking, sporopollenin 39 polymerization, microscopy. 2 https://mc06.manuscriptcentral.com/botany-pubs Page 3 of 32 Botany 40 Introduction 41 The evolution of land plants ~500 million years ago (Morris et al. 2018) required innovations to 42 counter challenges posed by dehydration, UV radiation and gravity. One such innovation was a 43 durable spore wall, which provided protection from dehydration and UV radiation. The bryophyte 44 spore wall is composed of a minimum of two layers, an inner intine and an outer exine. An 45 additional outermost perine layer is found in moss and fern spores (Brown and Lemmon 1990; 46 Wallace et al. 2011). Sporopollenin is the main polymeric constituent of the walls of spores (exine 47 and perine) and pollen grains (exine). It is chemically resistant and composed of polyhydroxylated 48 fatty acid derivatives and oxygenated aromatic compounds linked together by extensive ester and 49 ether bonds (Dominguez et al. 1999). A recent study provides chemical and spectroscopic evidence 50 that acetal linkages are also prevalent inDraft pine sporopollenin (Li et al. 2019). 51 Several enzymes involved in the biosynthesis of sporopollenin monomers and transcription 52 factors regulating their expression are known (Ariizumi and Toriyama 2011; Quilichini et al. 53 2015). In Arabidopsis, a fatty acyl reductase (MS2), two cytochrome P450-dependent fatty acid 54 hydroxylases (CYP703A2, CYP704B1), an acyl-CoA synthetase (ACOS5), two type III 55 polyketide synthases (PKSA, PKSB), and two tetraketide α-pyrone reductases (TKPR1, TKPR2) 56 participate in biosynthesis of sporopollenin monomers (Morant et al. 2007; de Azevedo Souza et 57 al. 2009; Dobritsa et al. 2009; Grienenberger et al. 2010; Kim et al. 2010; Chen et al. 2011). Also 58 in Arabidopsis, two transcription factors, ABORTED MICROSPORES and MALE STERILE 188, 59 form a regulatory feed-forward loop in which the former induces the latter, and they co-operatively 60 induce MS2, CYP703A2, PKSA and PKSB expression (Wang et al. 2018). Data from phylogenetic 61 and gene expression studies of Physcomitrella orthologs imply that the sporopollenin biosynthetic 62 pathway is widely conserved in land plants (Colpitts et al. 2011). This conclusion is strengthened 3 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 4 of 32 63 by the finding that Physcomitrella strains possessing deletion mutations of MS2 and PKSA/B 64 orthologs produce spores with defective walls (Wallace et al. 2015; Daku et al. 2016). However, 65 the enzymes that catalyze sporopollenin polymerization and deposition are yet to be discovered. 66 Chemical stability of lignin, suberin, and the polymeric matrices of the plant primary cell wall 67 is due largely to C–C and C–O (ether) bonds formed by oxidative coupling reactions (Bernards et 68 al. 1999; Burr and Fry 2009; Shigeto and Tsutsumi 2016). Class III peroxidases catalyze the 69 oxidative coupling reactions of lignin polymerization using H2O2 as oxidant. It is reasonable to 70 expect similar processes to occur in sporopollenin polymerization and its deposition in the walls 71 of spores and pollen grains. Matveyeva et al. (2012) reported evidence, using a fluorescent dye, –• 72 that the superoxide anion radical (O2 ) and probably other reactive oxygen species (ROS) are 73 present in the exine of tobacco microsporesDraft at the tetrad stage when sporopollenin polymerization 74 and deposition are occurring. 75 In culture, Physcomitrella sporophytic development, including sporogenesis, occurs when 76 sporophytes are submerged in water, thus enabling both chemical rescue and inhibitor studies. To 77 obtain evidence of the involvement of ROS in sporopollenin polymerization and spore wall 78 formation, we investigated the effects of ROS scavengers on the formation of spore walls by 79 exposing sporophytes containing developing spores to ascorbate (AsA), N,Nʹ-dimethylthiourea 80 (DMTU) and 4-hydroxy-Tempo (Tempol). AsA is a natural antioxidant, and DMTU and Tempol 81 are representative thiourea and nitroxide antioxidants, respectively. These scavengers are highly 82 soluble in water, less toxic and had already been studied in planta within the context of plant 83 developmental processes (Soule et al. 2007; Akram et al. 2017; Mei et al. 2017). 84 85 Materials and methods 4 https://mc06.manuscriptcentral.com/botany-pubs Page 5 of 32 Botany 86 Plant material, culture conditions and chemicals 87 The pabB4 strain of Physcomitrella patens (Hedw.) Bruch, Schimp & W. Gümbel (Ashton and 88 Cove 1977) was used in this study. PabB4 was obtained originally by NTG mutagenesis and shown 89 by conventional genetic analysis through sexual crossing to possess a single pab biochemical 90 mutation (Ashton and Cove 1977; Courtice et al. 1978). When grown on medium containing 91 adequate p-aminobenzoic acid (paba) (1.8 and 18 µM for gametophytes and sporophytes 92 respectively), the pabB4 control strain is phenotypically (i.e. morphologically and 93 developmentally) indistinguishable from the original Gransden wild type strain from which it was 94 derived. Like the original Gransden wild type, obtained from a single spore isolated from nature 95 by H.L.K. Whitehouse in 1962, it produces abundant sporophytes containing numerous viable 96 spores with normal spore coat ornamentationDraft and typical stratification of the spore wall into outer 97 perine, middle exine and inner intine layers (Ashton and Cove 1977; Courtice et al. 1978; Singer 98 et al. 2007; Singer and Ashton 2007; Daku et al. 2016). Gametophytic plants were grown 99 axenically in 30 mL glass tubes containing ABC medium (Knight et al. 1988) solidified with 1.5% 100 agar and supplemented with 1.8 µM paba. Cultures were maintained under continuous white light 101 (2540 mol cm2 s1) at 2022 C and 3050% relative humidity. To produce sporophytes, 2–3 102 month-old gametophytes were subjected to cold stress at 16 C for 3 weeks and then irrigated with 103 5 mM HEPES buffer (pH 8.0) containing 18 µM paba to facilitate fertilization and support growth 104 and development of the paba-requiring sporophytes. 105 AsA, DMTU and Tempol were purchased from Sigma-Aldrich (Oakville, ON, Canada). 106 107 Effects of ROS scavengers on the development of sporophytes and spores 108 At 0, 10 or 20 days post-irrigation (dpi), ROS scavengers were added at 0.1, 1 and 10 mM to the 5 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 6 of 32 109 irrigation solution in which plants had been submerged. By 35 dpi, sporophytes and the spores 110 within them had reached maturity (late orange stage) (Daku et al. 2016). For each treatment, three 111 culture tubes were used. Under the standard conditions, ~80 sporophytes were produced in each 112 tube. Two or more sporophytes from each of three culture tubes were collected and spores were 113 gently released into 200 L of water or PBS (phosphate buffered saline, pH 7.4). Spores were 114 immediately mixed by gentle pipetting and 10 L aliquots, each containing ~1000 spores, were 115 mounted on slides.
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