The YABBY gene SHATTERING1 controls activation rather than patterning of the abscission zone in Setaria viridis.
SHATTERING1
Setaria viridis
YABBY
abscission zone
auxin
chloroplast
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
received:
14
04
2023
accepted:
14
06
2023
medline:
22
9
2023
pubmed:
3
8
2023
entrez:
2
8
2023
Statut:
ppublish
Résumé
Abscission is predetermined in specialized cell layers called the abscission zone (AZ) and activated by developmental or environmental signals. In the grass family, most identified AZ genes regulate AZ anatomy, which differs among lineages. A YABBY transcription factor, SHATTERING1 (SH1), is a domestication gene regulating abscission in multiple cereals, including rice and Setaria. In rice, SH1 inhibits lignification specifically in the AZ. However, the AZ of Setaria is nonlignified throughout, raising the question of how SH1 functions in species without lignification. Crispr-Cas9 knockout mutants of SH1 were generated in Setaria viridis and characterized with histology, cell wall and auxin immunofluorescence, transmission electron microscopy, hormonal treatment and RNA-Seq analysis. The sh1 mutant lacks shattering, as expected. No differences in cell anatomy or cell wall components including lignin were observed between sh1 and the wild-type (WT) until abscission occurs. Chloroplasts degenerated in the AZ of WT before abscission, but degeneration was suppressed by auxin treatment. Auxin distribution and expression of auxin-related genes differed between WT and sh1, with the signal of an antibody to auxin detected in the sh1 chloroplast. SH1 in Setaria is required for activation of abscission through auxin signaling, which is not reported in other grass species.
Substances chimiques
Indoleacetic Acids
0
Transcription Factors
0
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
846-862Informations de copyright
© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation.
Références
Aloni R, Schwalm K, Langhans M, Ullrich CI. 2003. Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216: 841-853.
Atmodjo MA, Hao Z, Mohnen D. 2013. Evolving views of pectin biosynthesis. Plant Biology 64: 747-779.
Avni R, Nave M, Barad O, Baruch K, Twardziok SO, Gundlach H, Hale I, Mascher M, Spannagl M, Wiebe K et al. 2017. Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357: 93-97.
Avsian-Kretchmer O, Cheng J-C, Chen L, Moctezuma E, Sung ZR. 2002. Indole acetic acid distribution coincides with vascular differentiation pattern during Arabidopsis leaf ontogeny. Plant Physiology 130: 199-209.
Bailey TL, Johnson J, Grant CE, Noble WS. 2015. The MEME suite. Nucleic Acids Research 43: W39-W49.
Bar-Dror T, Dermastia M, Kladnik A, Znidaric MT, Novak MP, Meir S, Burd S, Philosoph-Hadas S, Ori N, Sonego L et al. 2011. Programmed cell death occurs asymmetrically during abscission in tomato. Plant Cell 23: 4146-4163.
Basu MM, González-Carranza ZH, Azam-Ali S, Tang S, Shahid AA, Roberts JA. 2013. The manipulation of auxin in the abscission zone cells of Arabidopsis flowers reveals that Indoleacetic acid signaling is a prerequisite for organ shedding. Plant Physiology 162: 96-106.
Boerjan W, Ralph J, Baucher M. 2003. Lignin biosynthesis. Plant Biology 54: 519-546.
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120.
Bowman JL. 2000. The YABBY gene family and abaxial cell fate. Current Opinion in Plant Biology 3: 17-22.
Dai M, Hu Y, Zhao Y, Liu H, Zhou D-X. 2007. A WUSCHEL-LIKE HOMEOBOX gene represses a YABBY gene expression required for rice leaf development. Plant Physiology 144: 380-390.
Dhonukshe P, Grigoriev I, Fischer R, Tominaga M, Robinson DG, Hašek J, Paciorek T, Petrášek J, Seifertová D, Tejos R et al. 2008. Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proceedings of the National Academy of Sciences, USA 105: 4489-4494.
Ding B, Li J, Gurung V, Lin Q, Sun X, Yuan Y. 2021. The leaf polarity factors SGS3 and YABBYs regulate style elongation through auxin signaling in Mimulus lewisii. New Phytologist 232: 2191-2206.
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. Star: ultrafast universal RNA-Seq aligner. Bioinformatics 29: 15-21.
Dong Y, Wang Y-Z. 2015. Seed shattering: from models to crops. Frontiers in Plant Science 6: 476.
van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J et al. 2011. Morphological classification of plant cell deaths. Cell Death & Differentiation 18: 1241-1246.
van Doorn WG, Woltering EJ. 2004. Senescence and programmed cell death: substance or semantics? Journal of Experimental Botany 55: 2147-2153.
Dunn KW, Kamocka MM, McDonald JH. 2011. A practical guide to evaluating colocalization in biological microscopy. American Journal of Physiology-Cell Physiology 300: C723-C742.
Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW. 2005. AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132: 4563-4574.
Ferrándiz C, Liljegren SJ, Yanofsky MF. 2000. Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289: 436-438.
Franco-Zorrilla JM, López-Vidriero I, Carrasco JL, Godoy M, Vera P, Solano R. 2014. DNA-binding specificities of plant transcription factors and their potential to define target genes. Proceedings of the National Academy of Sciences, USA 111: 2367-2372.
Fregeau JA, Wightman F. 1983. Natural occurrence and biosynthesis of auxins in chloroplast and mitochondrial fractions from sunflower leaves. Plant Science Letters 32: 23-34.
Gil-Humanes J, Wang Y, Liang Z, Shan Q, Ozuna CV, Sánchez-León S, Baltes NJ, Starker C, Barro F, Gao C et al. 2017. High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9. The Plant Journal 89: 1251-1262.
Hodge JG, Kellogg EA. 2016. Abscission zone development in Setaria viridis and its domesticated relative, Setaria italica. American Journal of Botany 103: 998-1005.
Juarez MT, Twigg RW, Timmermans MCP. 2004. Specification of adaxial cell fate during maize leaf development. Development 131: 4533-4544.
Kakei Y, Yamazaki C, Suzuki M, Nakamura A, Sato A, Ishida Y, Kikuchi R, Higashi S, Kokudo Y, Ishii T et al. 2015. Small-molecule auxin inhibitors that target YUCCA are powerful tools for studying auxin function. The Plant Journal 84: 827-837.
Kim J. 2014. Four shades of detachment: regulation of floral organ abscission. Plant Signaling & Behavior 9: e976154.
Kim J, Dotson B, Rey C, Lindsey J, Bleecker AB, Binder BM, Patterson SE. 2013. New clothes for the jasmonic acid receptor COI1: delayed abscission, meristem arrest and apical dominance. PLoS ONE 8: e60505.
Knapp E, Flores R, Scheiblin D, Scheiblin D, Modla S, Czymmek K, Czymmek K, Yusibov V. 2012. A cryohistological protocol for preparation of large plant tissue sections for screening intracellular fluorescent protein expression. BioTechniques 52: 31-37.
Konishi S, Izawa T, Lin SY, Ebana K, Fukuta Y, Sasaki T, Yano M. 2006. An SNP caused loss of seed shattering during rice domestication. Science 312: 1392-1396.
Lee J, Chen H, Lee G, Emonet A, Kim S, Shim D, Lee Y. 2022. MSD2-mediated ROS metabolism fine-tunes the timing of floral organ abscission in Arabidopsis. New Phytologist 235: 2466-2480.
Lee Y, Yoon TH, Lee J, Jeon SY, Lee JH, Lee MK, Chen H, Yun J, Oh SY, Wen X et al. 2018. A lignin molecular brace controls precision processing of cell walls critical for surface integrity in Arabidopsis. Cell 173: 1468-1480.
Lenser T, Theißen G. 2013. Conservation of fruit dehiscence pathways between Lepidium campestre and Arabidopsis thaliana sheds light on the regulation of INDEHISCENT. The Plant Journal 76: 545-556.
Leverone LA, Stroup TL, Caruso JL. 1991. Western blot analysis of cereal grain prolamins using an antibody to carboxyl-linked indoleacetic acid. Plant Physiology 96: 1076-1078.
Li C, Zhou A, Sang T. 2006. Rice domestication by reducing shattering. Science 311: 1936-1939.
Li F, Komatsu A, Ohtake M, Eun H, Shimizu A, Kato H. 2020. Direct identification of a mutation in OsSh1 causing non-shattering in a rice (Oryza sativa L.) mutant cultivar using whole-genome resequencing. Scientific Reports 10: 14936.
Li K, Reeve DW. 2005. Fluorescent labeling of lignin in the wood pulp fiber wall. Journal of Wood Chemistry and Technology 24: 169-181.
Li L-F, Olsen KM. 2016. To have and to hold: selection for seed and fruit retention during crop domestication. Current Topics in Developmental Biology 119: 63-109.
Liljegren SJ, Roeder AHK, Kempin SA, Gremski K, Østergaard L, Guimil S, Reyes DK, Yanofsky MF. 2004. Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116: 843-853.
Lin Z, Li X, Shannon LM, Yeh C-T, Wang ML, Bai G, Peng Z, Li J, Trick HN, Clemente TE et al. 2012. Parallel domestication of the Shattering1 genes in cereals. Nature Genetics 44: 720-724.
Liu H, Fang X, Zhou L, Li Y, Zhu C, Liu J, Song Y, Jian X, Xu M, Dong L et al. 2022. Transposon insertion drove the loss of natural seed shattering during Foxtail Millet domestication. Molecular Biology and Evolution 39: msac078.
Ljung K. 2013. Auxin metabolism and homeostasis during plant development. Development 140: 943-950.
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15. doi: 10.1186/s13059-014-0550-8.
Lv S, Wu W, Wang M, Meyer RS, Ndjiondjop M-N, Tan L, Zhou H, Zhang J, Fu Y, Cai H et al. 2017. Genetic control of seed shattering during African rice domestication. Nature Plants 4: 331-337.
Mamidi S, Healey A, Huang P, Grimwood J, Jenkins J, Barry K, Sreedasyam A, Shu S, Lovell JT, Feldman M et al. 2020. A genome resource for green millet, Setaria viridis, enables discovery of agronomically valuable loci. Nature Biotechnology 38: 1203-1210.
Mann DGJ, LaFayette PR, Abercrombie LL, King ZR, Mazarei M, Halter MC, Poovaiah CR, Baxter H, Shen H, Dixon RA et al. 2012. Gateway-compatible vectors for high-throughput gene functional analysis in switchgrass (Panicum virgatum L.) and other monocot species. Plant Biotechnology Journal 10: 226-236.
Márquez-López RE, Pérez-Hernández C, Ku-González Á, Galaz-Ávalos RM, Loyola-Vargas VM. 2018. Localization and transport of indole-3-acetic acid during somatic embryogenesis in Coffea canephora. Protoplasma 255: 695-708.
Mohnen D. 2008. Pectin structure and biosynthesis. Current Opinion in Plant Biology 11: 266-277.
Odonkor S, Choi S, Chakraborty D, Martinez-Bello L, Wang X, Bahri BA, Tenaillon MI, Panaud O, Devos KM. 2018. QTL mapping combined with comparative analyses identified candidate genes for reduced shattering in Setaria italica. Frontiers in Plant Science 9: 918.
O'Malley RC, Huang SC, Song L, Lewsey MG, Bartlett A, Nery JR, Galli M, Gallavotti A, Ecker JR. 2016. Cistrome and epicistrome features shape the regulatory DNA landscape. Cell 165: 1280-1292.
Patterson SE. 2001. Cutting loose. Abscission and dehiscence in Arabidopsis. Plant Physiology 126: 494-500.
Patterson SE, Bleecker AB. 2004. Ethylene-dependent and -independent processes associated with floral organ abscission in Arabidopsis. Plant Physiology 134: 194-203.
Pence VC, Caruso JL. 1987. Immunoassay methods of plant hormone analysis. In: Davies PJ, ed. Plant hormones and their role in plant growth and development. Dordrecht, the Netherland: Springer, 240-256.
Polko JK, Kieber JJ. 2019. The regulation of cellulose biosynthesis in plants. Plant Cell 31: 282-296.
Pourkheirandish M, Hensel G, Kilian B, Senthil N, Chen G, Sameri M, Azhaguvel P, Sakuma S, Dhanagond S, Sharma R et al. 2015. Evolution of the grain dispersal system in barley. Cell 162: 527-539.
Rosquete MR, Barbez E, Kleine-Vehn J. 2012. Cellular auxin homeostasis: gatekeeping Is housekeeping. Molecular Plant 5: 772-786.
Sakamoto M, Munemura I, Tomita R, Kobayashi K. 2008. Involvement of hydrogen peroxide in leaf abscission signaling, revealed by analysis with an in vitro abscission system in Capsicum plants. The Plant Journal 56: 13-27.
Salazar-Iribe A, De-la-Peña C. 2020. Auxins, the hidden player in chloroplast development. Plant Cell Reports 39: 1595-1608.
Sandberg G, Gardeström P, Sitbon F, Olsson O. 1990. Presence of indole-3-acetic acid in chloroplasts of Nicotiana tabacum and Pinus sylvestris. Planta 180: 562-568.
Sandberg G, Jensen E, Crozier A. 1982. Biosynthesis of indole-3-acetic acid in protoplasts, chloroplasts and a cytoplasmic fraction from barley (Hordeum vulgare L.). Planta 156: 541-545.
Sargent JA, Osborne DJ, Dunford SM. 1984. Cell separation and its hormonal control during fruit abscission in the Gramineae. Journal of Experimental Botany 35: 1663-1674.
Sarojam R, Sappl PG, Goldshmidt A, Efroni I, Floyd SK, Eshed Y, Bowman JL. 2010. Differentiating Arabidopsis shoots from leaves by combined YABBY activities. Plant Cell 22: 2113-2130.
Sauer M, Kleine-Vehn J. 2019. PIN-FORMED and PIN-LIKES auxin transport facilitators. Development 146: dev168088.
Scheller HV, Ulvskov P. 2010. Hemicelluloses. Annual Review of Plant Biology 61: 263-289.
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B et al. 2012. Fiji: an open-source platform for biological-image analysis. Nature Methods 9: 676-682.
Sexton R, Roberts JA. 1982. Cell biology of abscission. Annual Review of Plant Physiology 33: 133-162.
Shamimuzzaman M, Vodkin L. 2013. Genome-wide identification of binding sites for NAC and YABBY transcription factors and co-regulated genes during soybean seedling development by ChIP-Seq and RNA-Seq. BMC Genomics 14: 477.
Sun M, Li H, Li Y, Xiang H, Liu Y, He Y, Qi M, Li T. 2020. Tomato YABBY2b controls plant height through regulating indole-3-acetic acid-amido synthetase (GH3.8) expression. Plant Science 297: 110530.
Tanaka W, Toriba T, Ohmori Y, Yoshida A, Kawai A, Mayama-Tsuchida T, Ichikawa H, Mitsuda N, Ohme-Takagi M, Hirano H-Y. 2012. The YABBY Gene TONGARI-BOUSHI1 is involved in lateral organ development and maintenance of meristem organization in the rice spikelet. Plant Cell 24: 80-95.
Teale W, Palme K. 2017. Naphthylphthalamic acid and the mechanism of polar auxin transport. Journal of Experimental Botany 69: 303-312.
Van Eck J, Swartwood K, Pidgeon K, Maxson-Stein K. 2017. Agrobacterium tumefaciens-mediated transformation of Setaria viridis. In: Doust AD, Diao X, eds. Genetics and genomics of Setaria. Cham, Switzerland: Springer, 343-356.
Vanholme R, Meester BD, Ralph J, Boerjan W. 2019. Lignin biosynthesis and its integration into metabolism. Current Opinion in Biotechnology 56: 230-239.
Wehrens R, Buydens LMC. 2007. Self- and super-organizing maps in R: the kohonen package. Journal of Statistical Software 21: 1-19.
Weiser GC, Smith RL, Varnell RJ. 1979. Spikelet abscission in guineagrass as influenced by auxin and gibberellin 1. Crop Science 19: 231-235.
Weng J, Chapple C. 2010. The origin and evolution of lignin biosynthesis. New Phytologist 187: 273-285.
Woodson JD. 2022. Control of chloroplast degradation and cell death in response to stress. Trends in Biochemical Sciences 47: 851-864.
Wu T, Hu E, Xu S, Chen M, Guo P, Dai Z, Feng T, Zhou L, Tang W, Zhan L et al. 2021. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. The Innovations 2: 100141.
Yoon J, Cho L, Kim SL, Choi H, Koh H, An G. 2014. The BEL1-type homeobox gene SH5 induces seed shattering by enhancing abscission-zone development and inhibiting lignin biosynthesis. The Plant Journal 79: 717-728.
Yu Y, Beyene G, Villmer J, Duncan KE, Hu H, Johnson T, Doust AN, Taylor NJ, Kellogg EA. 2023. Grain shattering by cell death and fracture in Eragrostis tef. Plant Physiology 192: 222-239.
Yu Y, Hu H, Doust AN, Kellogg EA. 2020a. Divergent gene expression networks underlie morphological diversity of abscission zones in grasses. New Phytologist 225: 1799-1815.
Yu Y, Kellogg EA. 2018. Inflorescence abscission zones in grasses: diversity and genetic regulation. Annual Plant Reviews 1: 497-532.
Yu Y, Leyva P, Tavares RL, Kellogg EA. 2020b. The anatomy of abscission zones is diverse among grass species. American Journal of Botany 107: 549-561.
Yu Z, Zhang F, Friml J, Ding Z. 2022. Auxin signaling: research advances over the past 30 years. Journal of Integrative Plant Biology 64: 371-392.
Zhang J, Peer WA. 2017. Auxin homeostasis: the DAO of catabolism. Journal of Experimental Botany 68: 3145-3154.
Zhong R, Ye Z-H. 2015. Secondary cell walls: biosynthesis, patterned deposition and transcriptional regulation. Plant and Cell Physiology 56: 195-214.
Zhou Y, Lu D, Li C, Luo J, Zhu B-F, Zhu J, Shangguan Y, Wang Z, Sang T, Zhou B et al. 2012. Genetic control of seed shattering in rice by the APETALA2 transcription factor SHATTERING ABORTION1. Plant Cell 24: 1034-1048.