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AtGRDP1 Gene Encoding a Glycine-Rich Domain Protein Is Involved in Germination and Responds to ABA Signalling

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Abstract

Seed maturation and germination involve changes in gene expression, as well as physiological and metabolic events; however, much remains to be learned. In plants, abiotic stress affects germination, growth and development, significantly reducing productivity, and in some cases, causing plant death. AtGRDP1 is a novel protein that contains a short glycine-rich domain, a DUF1399 domain, and a putative RNP motif. Expression analysis showed that AtGRDP1 gene is modulated in response to NaCl, LiCl, mannitol, sorbitol, glucose, and exogenous ABA. In order to characterise the AtGRDP1 gene, null mutant and overerexpressing lines were obtained. The Atgrdp1-null mutant line showed an increased sensitivity to salt and osmotic stress in germination and cotyledon development, whereas 35S::AtGRDP1 overerexpressing lines resulted in increased tolerance to abiotic stress. Interestingly, 35S::AtGRDP1 overerexpressing lines showed resistance to ABA, resembling a well-known ABI phenotype, whereas the disruption of AtGRDP1 gene resulted in ABA hypersensitivity, mimicking the ABI3-overexpression phenotype. Furthermore, we analysed the ABI3 and ABI5 genes, which are central regulators in ABA signalling, in Atgrdp1-null mutant and 35S::AtGRDP1 overerexpressing lines. Under ABA treatments, Atgrdp1-null mutant seedlings showed higher ABI3 and ABI5 transcript levels, whereas in 35S::AtGRDP1 overexpressing line, the ABI3 and ABI5 transcripts were repressed. These results suggest that AtGRDP1 gene plays a regulatory role in ABA signalling and tolerance to abiotic stress.

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Abbreviations

ABI:

abscisic insensitive

ABI3 :

abscisic insensitive 3 gene

ABI5 :

abscisic insensitive 5 gene

AQP:

aquaporine

AtGRDP1 :

Arabidopsis thaliana glycine-rich domain protein 1

bZIP:

basic leucine zipper

DUF1399:

domain unknown function 1399

GRBP:

glycine RNA-binding protein

GRDP:

glycine-rich domain protein

GRP:

glycine-rich protein

Atgrdp1 :

insertional mutant of Atgrdp1

LEA:

late embryogenesis abundant

LTP:

lipid transfer proteins

HSPs:

heat shock proteins

35S::AtGRDP1 :

overexpression of AtGRDP1

qRT-PCR:

quantitative real-time PCR

RBP:

RNA-binding proteins

RNP:

RNA-binding motif

RRM-GRP:

RNA recognition motif GRPs

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Acknowledgements

This work was supported by the CONACYT (Investigación Ciencia Básica 2008-103106) funding. We are grateful to Jennifer Eckerly Goss and Raquel Jaramillo Monroy for a grammatical review, and M.C. Alicia Becerra Flora for their technical assistance. qRT-PCR analyses were carried out at LANBAMA, IPICYT.

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Authors and Affiliations

  1. Laboratorio de Estudios Moleculares de Respuesta a Estrés en Plantas, División de Biología Molecular, Instituto Potosino de Investigación Científica y Tecnológica AC, Camino a la Presa de San José 2055, AP 3-74 Tangamanga, C.P. 78216, San Luis Potosí, San Luis Potosí, México

    Aída Araceli Rodríguez-Hernández, María Azucena Ortega-Amaro & Juan Francisco Jiménez-Bremont

  2. Facultad de Agronomía, Universidad Autónoma de San Luis Potosí, Km.14.5 Carretera San Luis Potosí-Matehuala, C.P. 78321, Soledad de Graciano Sánchez, SLP, México

    Pablo Delgado-Sánchez

  3. Departamento de Biología Medioambiental, Centro de Investigaciones Biológicas-Consejo Superior de Investigaciones Científicas, Ramiro de Maeztu, 9, 28040, Madrid, Spain

    Julio Salinas

Authors
  1. Aída Araceli Rodríguez-Hernández
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  3. Pablo Delgado-Sánchez
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  5. Juan Francisco Jiménez-Bremont
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Correspondence to Juan Francisco Jiménez-Bremont.

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Supplementary Fig. S1

Multiple alignment of the amino acid sequences of the A. thaliana AtGRDP1 protein with putative orthologous of GRDP proteins in plants. AtGRDP1 (At2g22660) protein and 16 plant GRDP orthologues: Hordeum vulgare (55792422), Sorghum bicolor (242071757), Oryza sativa ssp. japonica (4680491), Arabidopsis lyrata (343817), Cucumis sativus (Cucsa.320670), Vitis vinifera (225469224), Manihot esculenta (cassava4.1_001458m.g), Ricinus communis (255572563), Populus trichocarpa (224133168), Prunus persica (ppa001356m.g), Glycine max (Glyma01g02400), Medicago truncatula (163889366), Mimulus guttatus (mgv1a001498m), Triticum aestivum (CBH32635), Setaria italica (Si005129m) and Zea mays (NP_001183164) sequences from Phytozome. Identical residues (asterisk) in the proteins and conserved amino acid substitutions (dots) are indicated. Dashes show gaps in the amino acid sequences introduced to optimise alignment. Characteristic motifs present in the GRDPs proteins are indicated: the Domain Unknown Function 1399 (DUF1399), the putative RNA binding motif (RNP) and Glycine-Rich Domain (GRD). (JPEG 441 kb)

High resolution image (TIFF 69123 kb)

Supplementary Fig. S2

Gene structure and expression of AtGRDP1 gene in Col-0 plantlets, Atgrdp1-null mutant, and 35S::AtGRDP1 overexpressing lines. A) Schematic representation of AtGRDP1 gene: 5′UTR (white rectangle), exons (grey rectangles), introns (lines), and T-DNA insertion (black triangle) of the Salk_079708 Atgrdp1-null mutant line. B) Expression levels of AtGRDP1 gene in Col-0 and Atgrdp1-null mutant plantlets by qRT-PCR. Value represents fold change in expression level of Atgrdp1-null mutant plantlets compared to Col-0 plantlets. C) Schematic representation of the 35S::AtGRDP1 construct in pMDC32 binary vector. RB, right border for T-DNA integration; 2x35S, cauliflower mosaic virus 35S promoter; attB1 and attB2 sites for recombination; AtGRDP1, A. thaliana GRDP1 cDNA; NosT, nopaline synthase (nos) terminator region; hpt, hygromycin resistance gene; LB, left border for T-DNA integration. D) Expression levels of AtGRDP1 gene in Col-0 and six 35S::AtGRDP1 (OE1, OE2, OE3, OE4, OE5, and OE6) overexpressing lines and four complement lines 35S::AtGRDP1/Atgrdp1 (C2, C3, C4, and C5) by qRT-PCR. Values represent fold change in expression level of transgenic plantlets compared to Col-0 plantlets. Quantification was based on a cycle threshold value, with the expression level of the AtGRDP1 normalised to the A. thaliana ubiquitin 5 (UBQ5) gene. Bars represent mean ± SE (n = 3). Asterisks indicate significant differences among Col-0, overexpressing and complement lines, according to the One-way ANOVA analysis and Tukey’s multiple comparison test (P < 0.05). (JPEG 26 kb)

High resolution image (TIFF 1291 kb)

Supplementary Fig. S3

Percentage of seed germination of A. thaliana Col-0 plantlets, Atgrdp1-null mutant and 35S::AtGRDP1 overexpressing lines under salt stress treatments. Seeds of each line were germinated: control, NaCl (100 and 175 mM), 13 mM LiCl, mannitol 4 % and sorbitol 4 %, seed germination percentages were evaluated at 4, 5, 6, and 7 days of treatments. Bars represent the means ± SE (n = 15) with five replicates. Asterisks indicate significant differences among Col-0, Atgrdp1-null mutant and 35S::AtGRDP1 overexpressing lines, according to the One-way ANOVA analysis and Tukey’s multiple comparison test (P < 0.05). (JPEG 86 kb)

High resolution image (TIFF 5620 kb)

Supplementary Fig. S4

Phenotype of A. thaliana Col-0 plants, Atgrdp1-null mutant and 35S::AtGRDP1 overexpressing lines under salt and osmotic stress treatments. A) Photograph of plantlets (without stress) and schematic representation of the lines arrangement are shown. Phenotype of cotyledons, and green cotyledons percentage was evaluated 16 days after seed germination on conditions of B) control, C) 100 mM NaCl, D) 125 mM NaCl, E) mannitol 4 %, F) sorbitol 4 %, G) glucose 4 %, H) 175 mM NaCl, 16 and 19 mM LiCl, and glucose 4 and 5 %. Bars represent the means ± SE (n = 15) with five replicates. Asterisks indicate significant differences among the Col-0, Atgrdp1-null mutant and 35S::AtGRDP1 overexpressing lines, according to the One-way ANOVA analysis and Tukey’s multiple comparison test (P < 0.05). (JPEG 66 kb)

High resolution image (TIFF 7645 kb)

Supplementary Fig. S5

Percentage of seed germination of A. thaliana Col-0 plants, Atgrdp1-null mutant, 35S::AtGRDP1-6 overexpressing line and (C2) complement line (35S::AtGRDP1/Atgrdp1-2) under abiotic and ABA treatment. Seeds of each line were germinated on 0.5 × MS medium supplemented with NaCl (100, 125, 150 and 175 mM), sorbitol (4, 5, 6 %), and ABA (5, 7 9 μM), seed germination percentages were evaluated at 4, 5, 6, and 7 days of treatments. Bars represent the means ± SE (n = 15) with five replicates. Asterisks indicate significant differences among Col-0, Atgrdp1-null mutant, 35S::AtGRDP1-6 and (C2) complement line (35S::AtGRDP1/Atgrdp1-3), according to the One-way ANOVA analysis and Tukey’s multiple comparison test (P < 0.05). (JPEG 85 kb)

High resolution image (TIFF 5284 kb)

Supplementary Fig. S6

Percentage of green cotyledons of A. thaliana Col-0 plants, Atgrdp1-null mutant, 35S::AtGRDP1-6 overexpressing line and (C2) complement line (35S::AtGRDP1/Atgrdp1-2) under abiotic and ABA treatment. A) Image of plantlets of each line (without stress) and schematic representation of the lines arrangement are shown. Plantlets of different genotypes were grown on 0.5 × MS medium containing 1.5 % sucrose. Green cotyledons percentage was evaluated 16 days after seed germination on conditions: B) 100, 125, 150 mM NaCl, C) sorbitol 4, 5, and 6 %, D) ABA 5, 7, and 9 μM. Photographs were taken on day 16. Bars represent the means ± SE (n = 15) with five replicates. Asterisks indicate significant differences among Col-0, Atgrdp1-null mutant, 35S::AtGRDP1-6 and (C2) complement line (35S::AtGRDP1/Atgrdp1-3), according to the One-way ANOVA analysis and Tukey’s multiple comparison test (P < 0.05). (JPEG 110 kb)

High resolution image (TIFF 12457 kb)

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Rodríguez-Hernández, A.A., Ortega-Amaro, M.A., Delgado-Sánchez, P. et al. AtGRDP1 Gene Encoding a Glycine-Rich Domain Protein Is Involved in Germination and Responds to ABA Signalling. Plant Mol Biol Rep 32, 1187–1202 (2014). https://doi.org/10.1007/s11105-014-0714-4

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