Editing of 1-aminocyclopropane-1-carboxylate oxidase genes negatively affects petunia seed germination.
1-Aminocyclopropane-1-carboxylic acid
Ethylene production
Gene expression
Gibberellic acid
Seedling growth
Journal
Plant cell reports
ISSN: 1432-203X
Titre abrégé: Plant Cell Rep
Pays: Germany
ID NLM: 9880970
Informations de publication
Date de publication:
Jan 2022
Jan 2022
Historique:
received:
19
08
2021
accepted:
11
10
2021
pubmed:
20
10
2021
medline:
9
2
2022
entrez:
19
10
2021
Statut:
ppublish
Résumé
Editing of ACO genes involved in ethylene biosynthesis pathway reduces ethylene production in petunia seeds and inhibits seed germination. Ethylene production in the seeds of Petunia hybrida cv. 'Mirage Rose' was associated with expression of 1-aminocyclopropane-1-carboxylic acid (ACC) oxidase (ACO) genes (PhACO1, PhACO3, and PhACO4). Suppression of their expression by ethylene inhibitor silver thiosulphate (STS) significantly reduced ethylene production and inhibited seed germination. When it was combined with ethylene precursor ACC, ethylene production was re-promoted via activation of the genes and higher seed germination was restored. This was confirmed using the mutants editing the genes and WT. In the present study, compared with wild type plants, three different mutants (phaco1, phaco3, and phaco4) showed significantly decreased germination percentages as well as delayed germination time and seedling growth. These reductions were associated with lighter seed weight, lower ACO transcript levels, and lower ethylene production in mutants. Inhibited seed germination owing to reduced ethylene production was further verified by the supplementation of exogenous ACC and gibberellic acid (GA
Identifiants
pubmed: 34665313
doi: 10.1007/s00299-021-02802-5
pii: 10.1007/s00299-021-02802-5
doi:
Substances chimiques
Ethylenes
0
Plant Proteins
0
ethylene
91GW059KN7
Amino Acid Oxidoreductases
EC 1.4.-
1-aminocyclopropane-1-carboxylic acid oxidase
EC 1.4.3.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
209-220Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Calvo AP, Nicolás C, Lorenzo O, Nicolás G, Rodríguez D (2004) Evidence for positive regulation by gibberellins and ethylene of ACC oxidase expression and activity during transition from dormancy to germination in Fagus sylvatica L. seeds. J Plant Growth Regul 23:44–53. https://doi.org/10.1007/s00344-004-0074-7
doi: 10.1007/s00344-004-0074-7
Cervantes E, Rodriguez A, Nicolas G (1994) Ethylene regulates the expression of a cysteine proteinase gene during germination of chickpea (Cicer arietinum L). Plant Mol Biol 25:207–215. https://doi.org/10.1007/BF00023238
doi: 10.1007/BF00023238
Chiwocha SDS, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, Ross ARS, Kermode AR (2005) The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. Plant J 42:35–48. https://doi.org/10.1111/j.1365-313X.2005.02359.x
doi: 10.1111/j.1365-313X.2005.02359.x
Chonowski M, Corbineau F, Côme D (1997) Physiological and biochemical changes induced in sunflower seeds by osmopriming and subsequent drying, storage and aging. Seed Sci Res 7:323–332. https://doi.org/10.1017/S096025850000372X
doi: 10.1017/S096025850000372X
Corbineau F, Xia Q, Bailly C, El-Maarouf-Bouteau H (2014) Ethylene, a key factor in the regulation of seed dormancy. Front Plant Sci 5:539. https://doi.org/10.1017/S096025850000372X
doi: 10.1017/S096025850000372X
pmcid: 4193209
De Martinis D, Mariani C (1999) Silencing gene expression of the ethylene-forming enzyme results in a reversible inhibition of ovule development in transgenic tobacco plants. Plant Cell 11:1061–1072. https://doi.org/10.1105/tpc.11.6.1061
doi: 10.1105/tpc.11.6.1061
pmcid: 144249
Fiorani F, Bogemann GM, Visser EJW, Lambers H, Voesenekm LACJ (2002) Ethylene emission and responsiveness to applied ethylene vary among Poa species that inherently differ in leaf elongation rates. Plant Physiol 129:1382–1390. https://doi.org/10.1104/pp.001198
doi: 10.1104/pp.001198
pmcid: 166531
Gorecki RJ, Ashino H, Satoh S, Esashi Y (1991) Ethylene production in pea and cocklebur seeds of differing vigour. J Exp Bot 42:407–414. https://doi.org/10.1093/jxb/42.3.407
doi: 10.1093/jxb/42.3.407
Hermann K, Meinhard J, Dobrev P, Linkies A, Pesek B, Heß B, Machackova I, Fischer U, Leubner-Metzger G (2007) 1-Aminocyclopropane-1-carboxylic acid and abscisic acid during the germination of sugar beet (Beta vulgaris L.)—a comparative study of fruits and seeds. J Exp Bot 58:3047–3060. https://doi.org/10.1093/jxb/erm162
doi: 10.1093/jxb/erm162
Huang LC, Lai UL, Yang SF, Chua MJ, Kuo CI, Tsai MF, Sun CW (2007) Delayed flower senescence of Petunia hybrida plants transformed with antisense broccoli ACC synthase and ACC oxidase genes. Postharvest Biol Technol 46:47–53. https://doi.org/10.1016/j.postharvbio.2007.03.015
doi: 10.1016/j.postharvbio.2007.03.015
Iglesias-Fernandez R, Matilla A (2009) After-ripening alters the gene expression pattern of oxidases involved in the ethylene and gibberellin pathways during the early imbibition of Sisymbrium officinale L. seeds. J Exp Bot 60:1645–1661. https://doi.org/10.1093/jxb/erp029
doi: 10.1093/jxb/erp029
pmcid: 2671615
Kawa-Miszczak L, Wêgrzynowicz-Lesiak E, Miszczak A, Saniewski M (2003) Effect of methyl jasmonate and ethylene on leaf growth, anthocyanin accumulation and CO
doi: 10.1007/PL00007009
Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44:283–307. https://doi.org/10.1146/annurev.pp.44.060193.001435
doi: 10.1146/annurev.pp.44.060193.001435
Kepczynski J (1986) Inhibition of Amaranthus caudatus seed germination by polyethylene glycol-6000 and abscisic acid and its reversal by ethephon or 1-aminocyclopropane-l-carboxylic acid. Physiol Plant 67:588–591. https://doi.org/10.1111/j.1399-3054.1986.tb05060.x
doi: 10.1111/j.1399-3054.1986.tb05060.x
Kepczynski J, Bialecka B (1994) Stimulatory effect of ethephon, ACC, gibberellin A3 and A4+7 on germination of methyl jasmonate inhibited Amaranthus caudatus L. seeds. Plant Growth Regul 14:211–216
doi: 10.1007/BF00024795
Kepczynski J, Kepczynska E (1997) Ethylene in seed dormancy and germination. Physiol Plant 101:720–726. https://doi.org/10.1111/j.1399-3054.1997.tb01056.x
doi: 10.1111/j.1399-3054.1997.tb01056.x
Khan AA (1994) ACC-derived ethylene production, a sensitive test for seed vigor. J Am Soc Hortic Sci 119:1083–1090. https://doi.org/10.21273/JASHS.119.5.1083
doi: 10.21273/JASHS.119.5.1083
Khan NA (2005) The influence of exogenous ethylene on growth and photosynthesis of mustard (Brassica juncea) following defoliation. Sci Hortic 105:499–505. https://doi.org/10.1016/j.scienta.2005.02.004
doi: 10.1016/j.scienta.2005.02.004
Khan NA, Mir MR, Nazar R, Singh S (2008) The application of ethephon (an ethylene releaser) increases growth, photosynthesis and nitrogen accumulation in mustard (Brassica juncea L.) under high nitrogen levels. Plant Biol 10:534–538. https://doi.org/10.1111/j.1438-8677.2008.00054.x
doi: 10.1111/j.1438-8677.2008.00054.x
Kucera B, Cohn MA, Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Sci Res 15:281–307. https://doi.org/10.1079/SSR2005218
doi: 10.1079/SSR2005218
Linkies A, Leubner-Metzger G (2012) Beyond gibberellins and abscisic acid: how ethylene and jasmonates control seed germination. Plant Cell Rep 31:253–270. https://doi.org/10.1007/s00299-011-1180-1
doi: 10.1007/s00299-011-1180-1
Linkies A, Müller K, Morris K, Turečková V, Wenk M, Cadman CSC, Corbineau F, Strnad M, Lynn JR, Finch-Savage WE, LeubnerMetzger G (2009) Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21:3803–3822. https://doi.org/10.1105/tpc.109.070201
doi: 10.1105/tpc.109.070201
pmcid: 2814513
Matilla AJ (2000) Ethylene in seed formation and germination. Seed Sci Res 10:111–126. https://doi.org/10.1017/S096025850000012X
doi: 10.1017/S096025850000012X
Matilla AJ, Matilla-Vazquez MA (2008) Involvement of ethylene in seed physiology. Plant Sci 175:87–89. https://doi.org/10.1016/j.plantsci.2008.01.014
doi: 10.1016/j.plantsci.2008.01.014
Naing AH, Kim CK (2020) Application of nano-silver particles to control the postharvest biology of cut flowers: a review. Sci Hortic 270:109463. https://doi.org/10.1016/j.scienta.2020.109463
doi: 10.1016/j.scienta.2020.109463
Naing AH, Lee K, Arun M, Lim KB, Kim CK (2017a) Characterization of the role of sodium nitroprusside (SNP) involved in long vase life of different carnation cultivars. BMC Plant Biol 17:149. https://doi.org/10.1186/s12870-017-1097-0
doi: 10.1186/s12870-017-1097-0
pmcid: 5586022
Naing AH, Win NM, Hang JS, Lim KB, Kim CK (2017b) Role of nano-silver and the bacterial strain Enterobacter cloacae in increasing vase life of cut carnation ‘Omea.’ Front Plant Sci 8:1590. https://doi.org/10.3389/fpls.2017.01590
doi: 10.3389/fpls.2017.01590
pmcid: 5601422
Nascimento WM, Cantlife DJ, Huber DJ (1999) Lettuce seed germination and endo-b-mannanase activity at high temperature is stimulated by ethylene. HortScience 34:513–519. https://doi.org/10.21273/HORTSCI.34.3.513B
doi: 10.21273/HORTSCI.34.3.513B
Ogawa M, Tanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591. https://doi.org/10.1105/tpc.011650
doi: 10.1105/tpc.011650
pmcid: 165403
Park DY, Naing AH, Ai TN, Han J, Kang IK, Kim CK (2017) Synergistic effect of nano silver with sucrose on extending vase life of the carnation cv. Edun Front Plant Sci 8:1601. https://doi.org/10.3389/fpls.2017.01601
doi: 10.3389/fpls.2017.01601
Petruzzelli L, Kunz S, Waldvogel R, Meins F, Leubner-Metzger G (1999) Distinct ethylene and tissue-specific regulation of B-1,3-glucanases and chitinases during pea seed germination. Planta 290:195–201. https://doi.org/10.1007/s004250050622
doi: 10.1007/s004250050622
Petruzzelli L, Coraggio I, Leubner-Metzger G (2000) Ethylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1-aminocyclo-propane-1-carboxylic acid oxidase. Planta 211:144–149. https://doi.org/10.1007/s004250000274
doi: 10.1007/s004250000274
Petruzzelli L, Sturaro M, Mainieri D, Leubner-Metzger G (2003) Calcium requirement for ethylene-dependent responses involving 1-aminocyclopropane-1-carboxylic acid oxidase in radicle tissues of germinated pea seeds. Plant Cell Environ 26:661–671. https://doi.org/10.1046/j.1365-3040.2003.01001.x
doi: 10.1046/j.1365-3040.2003.01001.x
Puga-Hermida MI, Gallardo M, Rodríguez-Gacio MD, Matilla AJ (2003) The heterogeneity of turnip-tops (Brassica rapa) seeds inside the silique affects germination, the activity of the final step of the ethylene pathway, and abscisic acid and polyamine content. Funct Plant Biol 30:767–775. https://doi.org/10.1071/FP03053
doi: 10.1071/FP03053
Rinaldi LMR (2000) Germination of seeds of olive (Olea europea L.) and ethylene production: effects of harvesting time and thidiazuron treatment. J Horticul Sci Biotechnol 75:727–732. https://doi.org/10.1080/14620316.2000.11511314
doi: 10.1080/14620316.2000.11511314
Rodríguez-Gacio MD, Nicolas C, Matilla AJ (2004) The final step of the ethylene biosynthesis pathway in turnip tops (Brassica rapa L. cv. Rapa): molecular characterization of the 1-aminocyclopropane-1-carboxylate oxidase BrACO1 throughout zygotic embryogenesis and germination of heterogeneous seeds. Physiol Plant 121:132–140. https://doi.org/10.1111/j.0031-9317.2004.00300.x
doi: 10.1111/j.0031-9317.2004.00300.x
Rudus I, Cembrowska-Lech D, Jaworska A, Kepczynski J (2019) Involvement of ethylene biosynthesis and perception during germination of dormant Avena fatua L. caryopses induced by KAR1 or GA3. Planta 249:719–738. https://doi.org/10.1007/s00425-018-3032-5
doi: 10.1007/s00425-018-3032-5
Samimy C, Taylor AG (1983) Influence of seed quality on ethylene production of germinating snap bean seeds. J Am Soc Hortic Sci 108:767–769
Siriwitayawan G, Geneve RL, Downie AB (2003) Seed germination of ethylene perception mutants of tomato and Arabidopsis. Seed Sci Res 13:303–314. https://doi.org/10.1079/SSR2003147
doi: 10.1079/SSR2003147
Tang X, Woodson WR (1996) Temporal and spatial expression of 1- aminocyclopropane-1-carboxylate oxidase mRNA following pollination of immature and mature petunia flowers. Plant Physiol 112:503–511. https://doi.org/10.1104/pp.112.2.503
doi: 10.1104/pp.112.2.503
pmcid: 157973
Tang X, Wang H, Brandt AS, Woodson WR (1993) Organization and structure of the 1-aminocyclopropane-1-carboxylate oxidase gene family from Petunia hybrida. Plant Mol Biol 23:1151–1164. https://doi.org/10.1007/BF00042349
doi: 10.1007/BF00042349
Wang WQ, Møller IM, Song SQ (2012) Proteomic analysis of embryonic axis of Pisum sativum seeds during germination and identification of proteins associated with loss of desiccation tolerance. J Proteom 77:68–86. https://doi.org/10.1016/j.jprot.2012.07.005
doi: 10.1016/j.jprot.2012.07.005
Xu J, Kang BC, Naing AH, Bae SJ, Kim JS, Kim H, Kim CK (2020) CRISPR/Cas9-mediated editing of 1-aminocyclopropane-1-carboxylate oxidase1 enhances Petunia flower longevity. Plant Biotechnol J 18:287–297. https://doi.org/10.1111/pbi.13197
doi: 10.1111/pbi.13197
Xu J, Naing AH, Bunch H, Jeong J, Kim H, Kim CK (2021) Enhancement of the flower longevity of petunia by CRISPR/Cas9-mediated targeted editing of ethylene biosynthesis genes. Postharvest Biol Technol 174:111460. https://doi.org/10.1016/j.postharvbio.2020.111460
doi: 10.1016/j.postharvbio.2020.111460
Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189. https://doi.org/10.1146/annurev.pp.35.060184.001103
doi: 10.1146/annurev.pp.35.060184.001103
Zapata PJ, Serrano M, Pretel MT, Amorós A, Botella MA (2004) Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci 167:781–788. https://doi.org/10.1016/j.plantsci.2004.05.014
doi: 10.1016/j.plantsci.2004.05.014