Abstract
Members of La-related protein (LARP) 1 family spread widely in various species, and they are involved in regulating many important biological processes in mammal, yeast, and fruit fly. However, functional research of LARP1s in plants is limited so far. In Arabidopsis, there are three members in LARP1 family, LARP1a, 1b, and 1c. Here, we found that the mutation of LARP1 genes delayed seed germination, implying that LARP1 proteins might be positive factors of seed germination in Arabidopsis. Moreover, the larp1 mutants showed more sensitive to abscisic acid (ABA) and paclobutrazol (PAC), as larp1 mutants displayed low rate of germination in medium contained ABA or PAC. Temporal and spatial expression analyses revealed that LARP1s were more abundant in seeds, especially in imbibed seeds. Subcellular localization analysis revealed that all LARP1 proteins could localize to the P-bodies, suggesting that LARP1s might play a role in RNA processes. Taken together, our results unravel new conserved functions of LARP1s in the regulation of Arabidopsis seed germination.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bai B, van der Horst S, Cordewener JHG, America TAHP, Hanson J, Bentsink L (2020) Seed-stored mRNAs that are specifically associated to monosomes are translationally regulated during germination. Plant Physiol 182:378–392. https://doi.org/10.1104/pp.19.00644
Barrero JM, Piqueras P, González-Guzmán M, Serrano R, Rodríguez PL, Ponce MR, Micol JL (2005) A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J Exp Bot 56:2071–2083. https://doi.org/10.1093/jxb/eri206
Basbouss-Serhal I, Pateyron S, Cochet F, Leymarie J, Bailly C (2017) 5’ to 3’ mRNA decay contributes to the regulation of Arabidopsis seed germination by dormancy. Plant Physiol 173:1709–1723. https://doi.org/10.1104/pp.16.01933
Bayfield MA, Yang RQ, Maraia RJ (2010) Conserved and divergent features of the structure and function of La and La-related proteins (LARPs). Biochim Biophys Acta 1799:365–378. https://doi.org/10.1016/j.bbagrm.2010.01.011
Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066. https://doi.org/10.1105/Tpc.9.7.1055
Bewley JD, Black M (1994) Seeds: germination, structure and composition. In: Bewley JD, Black M (eds) Seeds: physiology of development and germination. Springer, Boston, pp 1–33
Billey E et al (2021) LARP6C orchestrates posttranscriptional reprogramming of gene expression during hydration to promote pollen tube guidance. Plant Cell 33:2637–2661. https://doi.org/10.1093/plcell/koab131
Bogamuwa S, Jang JC (2013) The Arabidopsis tandem CCCH zinc finger proteins AtTZF4, 5 and 6 are involved in light-, abscisic acid- and gibberellic acid- mediated regulation of seed germination. Plant Cell Environ 36:1507–1519. https://doi.org/10.1111/pce.12084
Bousquet-Antonelli C, Deragon JM (2009) A comprehensive analysis of the La-motif protein superfamily. RNA 15:750–764. https://doi.org/10.1261/rna.1478709
Brocard-Gifford IM, Lynch TJ, Finkelstein RR (2003) Regulatory networks in seeds integrating developmental, abscisic acid, sugar, and light signaling. Plant Physiol 131:78–92. https://doi.org/10.1104/pp.011916
Burrows C et al (2010) The RNA binding protein Larp1 regulates cell division, apoptosis and cell migration. Nucleic Acids Res 38:5542–5553. https://doi.org/10.1093/nar/gkq294
Cao DN, Hussain A, Cheng H, Peng JR (2005) Loss of function of four DELLA genes leads to light- and gibberellin-independent seed germination in Arabidopsis. Planta 223:105–113. https://doi.org/10.1007/s00425-005-0057-3
Chen HH et al (2020) AtPER1 enhances primary seed dormancy and reduces seed germination by suppressing the ABA catabolism and GA biosynthesis in Arabidopsis seeds. Plant J 101:310–323. https://doi.org/10.1111/tpj.14542
Chen S et al (2021) Persulfidation-induced structural change in SnRK2.6 establishes intramolecular interaction between phosphorylation and persulfidation. Mol Plant 14:1814–1830. https://doi.org/10.1016/j.molp.2021.07.002
Deragon JM, Bousquet-Antonelli C (2015) The role of LARP1 in translation and beyond. Wires RNA 6:399–417. https://doi.org/10.1002/wrna.1282
Divi UK, Krishna P (2010) Overexpression of the brassinosteroid biosynthetic gene AtDWF4 in Arabidopsis seeds overcomes abscisic acid-induced inhibition of germination and increases cold tolerance in transgenic seedlings. J Plant Growth Regul 29:385–393. https://doi.org/10.1007/s00344-010-9150-3
Finkelstein RR (1994) Mutations at 2 new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J 5:765–771. https://doi.org/10.1046/j.1365-313X.1994.5060765.x
Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA2 domain protein. Plant Cell 10:1043–1054. https://doi.org/10.1105/Tpc.12.4.599
Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45. https://doi.org/10.1105/tpc.010441
Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415. https://doi.org/10.1146/annurev.arplant.59.032607.092740
Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:1251–1261. https://doi.org/10.1105/tpc.4.10.1251
Gotor C et al (2019) Signaling by hydrogen sulfide and cyanide through post-translational modification. J Exp Bot 70:4251–4265. https://doi.org/10.1093/jxb/erz225
Guan C, Wang X, Feng J, Hong S, Liang Y, Ren B, Zuo J (2014) Cytokinin antagonizes abscisic acid-mediated inhibition of cotyledon greening by promoting the degradation of ABSCISIC ACID INSENSITIVE5 protein in Arabidopsis. Plant Physiol 164:1515–1526. https://doi.org/10.1104/pp.113.234740
He R et al (2016) F-box gene FOA2 regulates GA- and ABA- mediated seed germination in Arabidopsis. Sci China Life Sci 59:1192–1194. https://doi.org/10.1007/s11427-016-0098-3
Jia J-J et al (2021) mTORC1 promotes TOP mRNA translation through site-specific phosphorylation of LARP1. Nucl Acids Res 49:3461–3489. https://doi.org/10.1093/nar/gkaa1239
Jiang J et al (2007) RNAi knockdown of Oryza sativa root meander curling gene led to altered root development and coiling which were mediated by jasmonic acid signalling in rice. Plant Cell Environ 30:690–699. https://doi.org/10.1111/j.1365-3040.2007.01663.x
Kalladan R, Lasky JR, Sharma S, Kumar MN, Juenger TE, Des Marais DL, Verslues PE (2019) Natural variation in 9-cis-epoxycartenoid dioxygenase 3 and ABA accumulation. Plant Physiol 179:1620–1631. https://doi.org/10.1104/pp.18.01185
Kim J, Somers DE (2010) Rapid assessment of gene function in the circadian clock using artificial microRNA in Arabidopsis mesophyll protoplasts. Plant Physiol 154:611–621
Koornneef M, Jorna ML, Derswan DLCB, Karssen CM (1982) The isolation of abscisic-acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L) Heynh. Theor Appl Genet 61:385–393. https://doi.org/10.1007/Bf00272861
Lee SC et al (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Gene Dev 16:646–658. https://doi.org/10.1101/Gad.969002
Leon-Kloosterziel KM et al (1996) Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant J 10:655–661. https://doi.org/10.1046/j.1365-313X.1996.10040655.x
Li Z-X, Zhang L-F, Li W-F, Qi L-W, Han S-Y (2017) MIR166a affects the germination of somatic embryos in Larixleptolepis by modulating IAA biosynthesis and signaling genes. J Plant Growth Regul 36:889–896. https://doi.org/10.1007/s00344-017-9693-7
Lizarrondo J, Dock-Bregeon A-C, Martino L, Conte MR (2021) Structural dynamics in the La-module of La-related proteins. RNA Biol 18:194–206. https://doi.org/10.1080/15476286.2020.1733799
Lopez-Molina L, Mongrand B, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328. https://doi.org/10.1046/j.1365-313X.2002.01430.x
Lorkovic ZJ (2009) Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci 14:229–236. https://doi.org/10.1016/j.tplants.2009.01.007
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068. https://doi.org/10.1126/science.1172408
Merret R et al (2013) XRN4 and LARP1 are required for a heat-triggered mRNA decay pathway involved in plant acclimation and survival during thermal stress. Cell Rep 5:1279–1293. https://doi.org/10.1016/j.celrep.2013.11.019
Nambara E, Marion-Poll A (2003) ABA action and interactions in seeds. Trends Plant Sci 8:213–217. https://doi.org/10.1016/S1360-1385(03)00060-8
Nelson SK, Steber CM (2018) Gibberellin hormone signal perception: down-regulating DELLA repressors of plant growth and development. In: Roberts JA (ed) Annual plant reviews online. John Wiley & Sons Ltd, Chichester, pp 153–187. https://doi.org/10.1002/9781119312994.apr0535
Nykamp K, Lee MH, Kimble J (2008) C-elegans La-related protein, LARP-1, localizes to germline P bodies and attenuates Ras-MAPK signaling during oogenesis. RNA 14:1378–1389. https://doi.org/10.1261/rna.1066008
Okamoto M et al (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107. https://doi.org/10.1104/pp.106.079475
Oñate-Sánchez L, Vicente-Carbajosa J (2008) DNA-free RNA isolation protocols for Arabidopsis thaliana, including seeds and siliques. BMC Res Notes 1:93. https://doi.org/10.1186/1756-0500-1-93
Parcy F, Valon C, Raynal M, Gaubiercomella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6:1567–1582. https://doi.org/10.1105/tpc.6.11.1567
Park SJ, Lee HJ, Lee K, Kang H (2020) A La-related protein LaRP6a delays flowering of Arabidopsis thaliana by upregulating FLC transcript levels. J Plant Biol 63:369–378. https://doi.org/10.1007/s12374-020-09261-7
Ruggiero B et al (2004) Uncoupling the effects of abscisic acid on plant growth and water relations. Analysis of sto1/nced3, an abscisic acid-deficient but salt stress-tolerant mutant in Arabidopsis. Plant Physiol 136:3134–3147. https://doi.org/10.1104/pp.104.046169
Rymarquis LA, Souret FF, Green PJ (2011) Evidence that XRN4, an Arabidopsis homolog of exoribonuclease XRN1, preferentially impacts transcripts with certain sequences or in particular functional categories. RNA 17:501–511. https://doi.org/10.1261/rna.2467911
Seo M et al (2006) Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J 48:354–366. https://doi.org/10.1111/j.1365-313X.2006.02881.x
Shu K et al (2013) ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. Plos Genet. https://doi.org/10.1371/journal.pgen.1003577
Shu K, Liu XD, Xie Q, He ZH (2016) Two faces of one seed: hormonal regulation of dormancy and germination. Mol Plant 9:34–45. https://doi.org/10.1016/j.molp.2015.08.010
Silva-Correia J, Freitas S, Tavares RM, Lino-Neto T, Azevedo H (2014) Phenotypic analysis of the Arabidopsis heat stress response during germination and early seedling development. Plant Methods 10:7. https://doi.org/10.1186/1746-4811-10-7
Souret FF, Kastenmayer JP, Green PJ (2004) AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol Cell 15:173–183. https://doi.org/10.1016/j.molcel.2004.06.006
Tcherkezian J, Cargnello M, Romeo Y, Huttlin EL, Lavoie G, Gygi SP, Roux PP (2014) Proteomic analysis of cap-dependent translation identifies LARP1 as a key regulator of 5 ’ TOP mRNA translation. Gene Dev 28:357–371. https://doi.org/10.1101/gad.231407.113
Tyler L, Thomas SG, Hu JH, Dill A, Alonso JM, Ecker JR, Sun TP (2004) DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019. https://doi.org/10.1104/pp.104.039578
Wang ZP, Xing HL, Dong L, Zhang HY, Han CY, Wang XC, Chen QJ (2015) Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol. https://doi.org/10.1186/S13059-015-0715-0
Wang Z et al (2020) Counteraction of ABA-mediated inhibition of seed germination and seedling establishment by ABA signaling terminator in Arabidopsis. Mol Plant 13:1284–1297. https://doi.org/10.1016/j.molp.2020.06.011
Weber C, Nover L, Fauth M (2008) Plant stress granules and mRNA processing bodies are distinct from heat stress granules. Plant J 56:517–530. https://doi.org/10.1111/j.1365-313X.2008.03623.x
Weitbrecht K, Müller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62:3289–3309. https://doi.org/10.1093/jxb/err030
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2:e718–e718. https://doi.org/10.1371/journal.pone.0000718
Wolin SL, Cedervall T (2002) The LA protein. Annu Rev Biochem 71:375–403. https://doi.org/10.1146/annurev.biochem.71.090501.150003
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251. https://doi.org/10.1146/annurev.arplant.59.032607.092804
Yamauchi Y, Ogawa M, Kuwahara A, Hanada A, Kamiya Y, Yamaguchi S (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell 16:367–378. https://doi.org/10.1105/tpc.018143
Yamauchi Y et al (2007) Contribution of gibberellin deactivation by AtGA2ox2 to the suppression of germination of dark-imbibed Arabidopsis thaliana seeds. Plant Cell Physiol 48:555–561. https://doi.org/10.1093/pcp/pcm023
Yan CX, Yan ZY, Wang YZ, Yan XY, Han YZ (2014) Tudor-SN, a component of stress granules, regulates growth under salt stress by modulating GA20ox3 mRNA levels in Arabidopsis. J Exp Bot 65:5933–5944. https://doi.org/10.1093/jxb/eru334-
Yan Z, Jia J, Yan X, Shi H, Han Y (2017) Arabidopsis KHZ1 and KHZ2, two novel non-tandem CCCH zinc-finger and K-homolog domain proteins, have redundant roles in the regulation of flowering and senescence. Plant Mol Biol 95:549–565. https://doi.org/10.1007/s11103-017-0667-8
Yan Z, Shi H, Liu Y, Jing M, Han Y (2019) KHZ1 and KHZ2, novel members of the autonomous pathway, repress the splicing efficiency of FLC pre-mRNA in Arabidopsis. J Exp Bot 71:1375–1386. https://doi.org/10.1093/jxb/erz499
Yang M, Han X, Yang J, Jiang Y, Hu Y (2021) The Arabidopsis circadian clock protein PRR5 interacts with and stimulates ABI5 to modulate abscisic acid signaling during seed germination. Plant Cell 33:3022–3041. https://doi.org/10.1093/plcell/koab168
Yasmeen R, Siddiqui ZS (2017) Ameliorative effects of Trichoderma harzianum on monocot crops under hydroponic saline environment. Acta Physiol Plant 40:4. https://doi.org/10.1007/s11738-017-2579-2
Yu LH, Wu J, Zhang ZS, Miao ZQ, Zhao PX, Wang Z, Xiang CB (2017) Arabidopsis MADS-box transcription factor AGL21 acts as environmental surveillance of seed germination by regulating ABI5 expression. Mol Plant 10:834–845. https://doi.org/10.1016/j.molp.2017.04.004
Zanin E, Pacquelet A, Scheckel C, Ciosk R, Gotta M (2010) LARP-1 promotes oogenesis by repressing fem-3 in the C. elegans germline. J Cell Sci 123:2717–2724. https://doi.org/10.1242/jcs.066761
Zhang BY, Jia JH, Yang M, Yan CX, Han YZ (2012) Overexpression of a LAM domain containing RNA-binding protein LARP1c induces precocious leaf senescence in Arabidopsis. Mol Cells 34:367–374. https://doi.org/10.1007/s10059-012-0111-5
Zheng L, Yang J, Chen Y, Ding L, Wei J, Wang H (2021) An improved and efficient method of Agrobacterium syringe infiltration for transient transformation and its application in the elucidation of gene function in poplar. BMC Plant Biol 21:54. https://doi.org/10.1186/s12870-021-02833-w
Zhong CM, Xu H, Ye ST, Wang SY, Li LF, Zhang SC, Wang XJ (2015) Gibberellic acid-stimulated Arabidopsis6 serves as an integrator of gibberellin, abscisic acid, and glucose signaling during seed germination in Arabidopsis. Plant Physiol 169:2288–2303. https://doi.org/10.1104/pp.15.00858
Acknowledgements
We thank Dr. Markus Fauth of Johann Wolfgang Goethe-University Frankfurt for providing the RFP-DCP1 vector. We thank Dr. Xinping Yang (postdoctor of Wageningen University & Research) for language help. The study was supported by a grant from the National Natural Science Foundation of China (No. 31570254).
Author information
Authors and Affiliations
Contributions
YH conceived the research and supervised the experiment. ZY designed and performed experiments and prepared the figures. MJ and BZ performed the experiments. HS, XJ, XY, and TG provided technical assistance. ZY and YH wrote the manuscript.
Corresponding authors
Ethics declarations
Conflict of Interest
The authors have no conflicts of interest to declare.
Additional information
Handling Editor: Pramod Kumar Nagar
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yan, Z., Jing, M., Zhang, B. et al. The Arabidopsis LARP1s are Involved in Regulation of Seed Germination. J Plant Growth Regul 42, 1775–1788 (2023). https://doi.org/10.1007/s00344-022-10659-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-022-10659-5