Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-25T17:10:10.972Z Has data issue: false hasContentIssue false

A role for PM19-Like 1 in seed dormancy in Arabidopsis

Published online by Cambridge University Press:  26 July 2019

Jose M. Barrero*
Affiliation:
CSIRO Agriculture and Food, Canberra, ACT 2601, Australia
Marie M. Dorr
Affiliation:
CSIRO Agriculture and Food, Canberra, ACT 2601, Australia
Mark J. Talbot
Affiliation:
CSIRO Agriculture and Food, Canberra, ACT 2601, Australia
Shinnosuke Ishikawa
Affiliation:
Graduate School of Bio-Applications and Systems Engineering, Tokyo University of Agriculture and Technology, Koganei, Tokyo 184-8588, Japan
Taishi Umezawa
Affiliation:
Graduate School of Bio-Applications and Systems Engineering, Tokyo University of Agriculture and Technology, Koganei, Tokyo 184-8588, Japan
Rosemary G. White
Affiliation:
CSIRO Agriculture and Food, Canberra, ACT 2601, Australia
Frank Gubler
Affiliation:
CSIRO Agriculture and Food, Canberra, ACT 2601, Australia
*
*Author for correspondence: Jose Barrero, Email: jose.barrero@csiro.au

Abstract

The understanding of the genetic basis of grain dormancy in wheat has rapidly improved in the last few years, and a number of genes have been identified related to that trait. We recently identified the wheat genes TaPM19-A1 and -A2 and we have now taken the first step towards understanding the role of this class of genes in seeds. By investigating the Arabidopsis homologous PM19-Like 1 (PM19L1) we have found that it has a seed-specific expression pattern and, while its expression is higher in dormant than in non-dormant seeds, knock-out mutations produced seeds with increased dormancy. Not only primary dormancy, but also secondary dormancy in response to high temperature was increased by the loss-of-function. We have also examined the function of PM19L1 by localizing the PM19 protein primarily to the cotyledon cells in seeds, possibly in membranes. By investigating the co-expression network of this gene we have found that it is connected to a small group of abscisic acid (ABA)-induced seed maturation and storage-related genes. The function of PM19L1 represents a good opportunity to explore the interactions of key factors that can influence seed dormancy such as ABA, temperature and membrane properties.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Current address: Universite Laval, Quebec, Canada.

§

Current address: Sunrice, Leeton, NSW, Australia.

References

Alonso, JM, Stepanova, AN, Leisse, TJ, Kim, CJ, Chen, H, Shinn, P, Stevenson, DK, Zimmerman, J, Barajas, P, Cheuk, R, Gadrinab, C, Heller, C, Jeske, A, Koesema, E, Meyers, CC, Parker, H, Prednis, L, Ansari, Y, Choy, N, Deen, H, Geralt, M, Hazari, N, Hom, E, Karnes, M, Mulholland, C, Ndubaku, R, Schmidt, I, Guzman, P, Aguilar-Henonin, L, Schmid, M, Weigel, D, Carter, DE, Marchand, T, Risseeuw, E, Brogden, D, Zeko, A, Crosby, WL, Berry, CC and Ecker, JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653657.Google Scholar
Alsaif, OM (2013) The PM19 Protein: a Functional Analysis in Arabidopsis thaliana. PhD thesis, University Edinburgh, UK.Google Scholar
Ashburner, M, Ball, CA, Blake, JA, Botstein, D, Butler, H, Cherry, JM, Davis, AP, Dolinski, K, Dwight, SS, Eppig, JT, Harris, MA, Hill, DP, Issel-Tarver, L, Kasarskis, A, Lewis, S, Matese, JC, Richardson, JE, Ringwald, M, Rubin, GM and Sherlock, G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics 25, 2529.Google Scholar
Bassel, GW, Lan, H, Glaab, E, Gibbs, DJ, Gerjets, T, Krasnogor, N, Bonner, AJ, Holdsworth, MJ and Provart, NJ (2011) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proceedings of the National Academy of Sciences of the USA 108, 97099714.Google Scholar
Barrero, JM, Cavanagh, C, Verbyla, KL, Tibbits, JF, Verbyla, AP, Huang, BE, Rosewarne, GM, Stephen, S, Wang, P, Whan, A, Rigault, P, Hayden, MJ and Gubler, F (2015). Transcriptomic analysis of wheat near-isogenic lines identifies PM19-A1 and A2 as candidates for a major dormancy QTL. Genome Biology 16, 93102.Google Scholar
Barrero, JM, Downie, AB, Xu, Q and Gubler, F (2014). A role for barley CRYPTOCHROME1 in light regulation of grain dormancy and germination. Plant Cell 26, 1094–104.Google Scholar
Barrero, JM, Millar, AA, Griffiths, J, Czechowski, T, Scheible, WR, Udvardi, M, Reid, JB, Ross, JJ, Jacobsen, JV and Gubler, F (2010) Gene expression profiling identifies two regulatory genes controlling dormancy and ABA sensitivity in Arabidopsis seeds. Plant Journal 61, 611622.Google Scholar
Bentsink, L, Jowett, J, Hanhart, CJ and Koornneef, M (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proceedings of the National Academy of Sciences of the USA 103, 1704217047.Google Scholar
Black, M, Bewley, JD and Halmer, P (2006) The Encyclopedia of Seeds, Science, Technology and Uses. Wallingford, UK: CABI Publishers.Google Scholar
Brill, E, van Thournout, M, White, RG, Llewellyn, D, Campbell, PM, Engelen, S, Ruan, Y.-L., Arioli, T and Furbank, RT (2011) A novel isoform of sucrose synthase is targeted to the cell wall during secondary cell wall synthesis in cotton fiber. Plant Physiology 157, 4045.Google Scholar
Chang, SJ, Puryear, J and Cairney, J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Molecular Biology Reporter 11, 113116.Google Scholar
Chapman, KD, Dyer, JM and Mullen, RT (2012) Biogenesis and functions of lipid droplets in plants: thematic review series: lipid droplet synthesis and metabolism: from yeast to man. Journal of Lipid Research 53, 215226.Google Scholar
Chen, H, Lan, H, Huang, P, Zhang, Y, Yuan, X, Huang, X, Huang, J and Zhang, H (2015) Characterization of OsPM19L1 encoding an AWPM-19-like family protein that is dramatically induced by osmotic stress in rice. Genetics and Molecular Research 14, 11994–2005.Google Scholar
Chen, T, Nayak, N, Majee, SM, Lowenson, J, Schafermeyer, KR, Eliopoulos, AC, Lloyd, TD, Dinkins, R, Perry, SE, Forsthoefel, NR, Clarke, SG, Vernon, DM, Zhou, ZS, Rejtar, T and Downie, AB (2010) Substrates of the Arabidopsis thaliana protein isoaspartyl methyltransferase1 identified using phage display and biopanning. Journal of Biological Chemistry 285, 3728137292.Google Scholar
Clough, SJ and Bent, AF (1998) Floral dip: a simplified method for Agrobacterium- mediated transformation of Arabidopsis thaliana. Plant Journal 16, 735743.Google Scholar
Dekkers, BJ, He, H, Hanson, J, Willems, LA, Jamar, DC, Cueff, G, Rajjou, L, Hilhorst, HWM and Bentsink, L (2016) The Arabidopsis DELAY OF GERMINATION 1 gene affects ABSCISIC ACID INSENSITIVE 5 (ABI5) expression and genetically interacts with ABI3 during Arabidopsis seed development. Plant Journal 85, 451465.Google Scholar
Eamens, AL, McHale, M and Waterhouse, PM (2014) The use of artificial microRNA technology to control gene expression in Arabidopsis thaliana. Methods in Molecular Biology 1062, 211224.Google Scholar
Eamens, AL, Smith, NA, Curtin, SJ, Wang, M-B and Waterhouse, PM (2009). The Arabidopsis thaliana double stranded RNA binding protein DRB1 directs guide strand selection from microRNA duplexes. RNA 15, 22192235.Google Scholar
Finkelstein, R and Lynch, T (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 2, 599609.Google Scholar
Giraudat, J, Hauge, BM, Valon, C, Smalle, J, Parcy, F and Goodman, HM (1992) Isolation of the Arabidopsis-Abi3 gene by positional cloning. Plant Cell 4, 12511261.Google Scholar
Gleave, AP (1992) A versatile binary vector system with a T-DNA organizational-structure conducive to efficient integration of cloned DNA into the plant genome. Plant Molecular Biology 20, 12031207.Google Scholar
Gubler, F, Hughes, T, Waterhouse, P and Jacobsen, J (2008) Regulation of dormancy in barley by blue light and after-ripening: effects on abscisic acid and gibberellin metabolism. Plant Physiology 147, 886896.Google Scholar
Guo, WJ and Ho, TH (2008) An abscisic acid-induced protein, HVA22, inhibits gibberellin-mediated programmed cell death in cereal aleurone cells. Plant Physiology 147, 17101722.Google Scholar
Griffiths, J, Barrero, JM, Taylor, J, Helliwell, CA and Gubler, F (2011) ALTERED MERISTEM PROGRAM 1 is involved in development of seed dormancy in Arabidopsis. PLoS One 65, e20408.Google Scholar
Khan, JA, Wang, Q, Sjölund, RD, Schulz, A and Thompson, GA (2007) An early nodulin-like protein accumulates in the sieve element plasma membrane of Arabidopsis. Plant Physiology 143, 15761589.Google Scholar
Koike, M, Takezawa, D, Arakawa, K and Yoshida, S (1997) Accumulation of 19-kDa plasma membrane polypeptide during induction of freezing tolerance in wheat suspension-cultured cells by abscisic acid. Plant & Cell Physiology 38, 707716.Google Scholar
Li, Y-C, Zhang, C-Y, Zhang, N, Meng, F-R, Ren, J-P, Niu, H-B, Wang, X and Yin, J (2012) Cloning of a plasma membrane protein gene TaPM19-1 and its response to abiotic stresses in wheat. China Agriculture Science 45, 25022509.Google Scholar
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402408.Google Scholar
Lopez-Molina, L, Mongrand, S, McLachlin, DT, Chait, BT and Chua, NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant Journal 32, 317328.Google Scholar
Mansfield, SG and Briarty, LG (1992) Cotyledon cell development in Arabidopsis thaliana during reserve deposition. Canadian Journal of Botany 70, 151164.Google Scholar
Mangelsen, E, Kilian, J, Harter, K, Jansson, C, Wanke, D and Sundberg, E (2011) Transcriptome analysis of high-temperature stress in developing barley caryopses: early stress responses and effects on storage compound biosynthesis. Molecular Plant 4, 97115.Google Scholar
Martel, C, Blair, LK and Donohue, K (2018) PHYD prevents secondary dormancy establishment of seeds exposed to high temperature and is associated with lower PIL5 accumulation. Journal of Experimental Botany 69, 31573169.Google Scholar
Mi, H, Huang, X, Muruganujan, A, Tang, H, Mills, C, Kang, D and Thomas, PD (2017) PANTHER version 11: expanded annotation data from Gene Ontology and Reactome pathways, and data analysis tool enhancements. Nucleic Acids Research 45, D183D189.Google Scholar
Millar, AA, Jacobsen, JV, Ross, JJ, Helliwell, CA, Poole, AT, Scofield, G, Reid, JB and Gubler, F (2006) Seed dormancy and ABA metabolism in Arabidopsis and barley: the role of ABA 8'-hydroxylase. Plant Journal 45, 942954.Google Scholar
Mönke, G, Seifert, M, Keilwagen, J, Mohr, M, Grosse, I, Hähnel, U, Junker, A, Weisshaar, B, Conrad, U, Bäumlein, H and Altschmied, L (2012) Toward the identification and regulation of the Arabidopsis thaliana ABI3 regulon. Nucleic Acids Research 40, 82408254.Google Scholar
Naramoto, S, Kleine-Vehn, J, Robert, S, Fujimoto, M, Dainobu, T, Paciorek, T, Ueda, T, Nakano, A, Van Montagu, MCE, Fukuda, H and Friml, J (2010) ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proceedings of the National Academy of Sciences of the USA 107, 2189021895.Google Scholar
Penfield, S, Rylott, EL, Gilday, AD, Graham, S, Larson, TR and Graham, IA (2004) Reserve mobilization in the Arabidopsis endosperm fuels hypocotyl elongation in the dark, is independent of abscisic acid, and requires PHOSPHOENOLPYRUVATE CARBOXYKINASE1. Plant Cell 16, 27052718.Google Scholar
Penfield, S, Josse, EM, Kannangara, R, Gilday, AD, Halliday, KJ and Graham, IA (2005) Cold and light control seed germination through the bHLH transcription factor SPATULA. Current Biology 15, 19982006.Google Scholar
Ranford, JC, Bryce, JH and Morris, PC (2002) PM19, a barley (Hordeum vulgare L.) gene encoding a putative plasma membrane protein, is expressed during embryo development and dormancy. Journal of Experimental Botany 53, 147148.Google Scholar
Shorinola, O, Balcárková, B, Hyles, J, Tibbits, JFG, Hayden, MJ, Holušova, K, Valárik, M, Distelfeld, A, Torada, A, Barrero, JM and Uauy, C (2017) Haplotype analysis of the pre-harvest sprouting resistance locus Phs-A1 reveals a causal role of TaMKK3-A in global germplasm. Frontiers in Plant Science 8, 1555.Google Scholar
Torada, A, Koike, M, Ogawa, T, Takenouchi, Y, Tadamura, K, Wu, J, Matsumoto, T, Kawaura, K and Ogihara, Y (2016). A causal gene for seed dormancy on wheat chromosome 4A encodes a MAP kinase kinase. Current Biology 26, 782787.Google Scholar
Vaistij, FE, Gan, Y, Penfield, S, Gilday, AD, Dave, A, He, Z, Josse, EM, Choi, G, Halliday, KJ and Graham, IA (2013) Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA. Proceedings of the National Academy of Sciences of the USA 110, 1086610871.Google Scholar
Vermachova, M, Purkrtova, Z, Santrucek, J, Jolivet, P, Chardot, T and Kodicek, M (2011) New protein isoforms identified within Arabidopsis thaliana seed oil bodies combining chymotrypsin/trypsin digestion and peptide fragmentation analysis. Proteomics 11, 34303434.Google Scholar
Yao, L, Cheng, X, Gu, Z, Huang, W, Li, S, Wang, L, Wang, YF, Xu, P, Ma, H and Ge, X (2018) The AWPM-19 family protein OsPM1 mediates abscisic acid influx and drought response in rice. Plant Cell 30, 12581276.Google Scholar
Yoshida, T, Fujita, Y, Sayama, H, Kidokoro, S, Maruyama, K, Mizoi, J, Shinozaki, K and Yamaguchi-Shinozaki, K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant Journal 61, 672685.Google Scholar
Zhao, P, Liu, F, Ma, M, Gong, J, Wang, Q, Jia, P, Zheng, G and Liu, H (2011). Overexpression of AtLEA3-3 confers resistance to cold stress in Escherichia coli and provides enhanced osmotic stress tolerance and ABA sensitivity in Arabidopsis thaliana. Molecular Biology 45, 785796.Google Scholar
Supplementary material: File

Barrero et al. supplementary material

Table S1

Download Barrero et al. supplementary material(File)
File 16.1 KB