Abstract
Main conclusion
An amaranth DGR gene, induced under abiotic stress, modifies cell wall structure and causes hypersensitivity to ABA and salt when overexpressed in Arabidopsis.
DUF642 is a highly conserved plant-specific family of unknown cell wall-associated proteins. The AhDGR2 gene, coding for a DUF642 protein, was significantly induced in grain amaranth (Amaranthus hypochondriacus) plants subjected to water-deficit and salinity stress, thereby suggesting its participation in abiotic stress tolerance in this plant. A role in development was also inferred from the higher AhDGR2 expression rates detected in young tissues. Subsequent overexpression of AhDGR2 in transgenic Arabidopsis plants (OE-AhDGR2) supported its possible role in development processes. Thus, OE-AhDGR2 plants generated significantly longer roots when grown in normal MS medium. However, they showed a hypersensitivity to increasing concentrations of abscisic acid or NaCl in the medium, as manifested by shorter root length, smaller and slightly chlorotic rosettes, as well as highly reduced germination rates. Contrary to expectations, OE-AhDGR2 plants were intolerant to abiotic stress. Moreover, cell walls in transgenic plants were thinner, in leaves, and more disorganized, in roots, and had significantly modified pectin levels. Lower pectin methylesterase activity detected in leaves of OE-AhDGR2 plants, but not in roots, was contrary to previous reports associating DUF642 proteins and decreased pectin esterification levels in cell walls. Nonetheless, microarray data identified candidate genes whose expression levels explained the phenotypes observed in leaves of OE-AhDGR2 plants, including several involved in cell wall integrity and extension, growth and development, and resistance to abiotic stress. These results support the role of DUF642 proteins in cell wall-related processes and offer novel insights into their possible role(s) in plants.
Similar content being viewed by others
Abbreviations
- DGR:
-
DUF642 L-GalL-responsive gene
- DUF:
-
Domain of unknown function
- SOD:
-
Superoxide dismutase
- PME:
-
Pectin methylesterase
References
Abraham-Juárez MJ, Martínez-Hernández A, Leyva-González MA, Herrera-Estrella L, Simpson J (2010) Class I KNOX genes are associated with organogenesis during bulbil formation in Agave tequilana. J Exp Bot 61:4055–4067
Abrahams S, Hayes C, Watson J (1995) Expression patterns of three genes in the stem of lucerne (Medicago sativa). Plant Mol Biol 27:513–528
Anderson CT (2016) We be jammin’: an update on pectin biosynthesis, trafficking and dynamics. J Exp Bot 67:495–502
Ashapkin VV, Kutueva LI, Vanyushin BF (2016) Plant DNA methyltransferase genes: multiplicity, expression, methylation patterns. Biochemistry 81:141–151 (Moscow)
Borecký J, Maia IG, Costa ADT, Ježek P, Chaimovich H, Andrade PBM, Vercesi AE, Arruda P (2001) Functional reconstitution of Arabidopsis thaliana plant uncoupling mitochondrial protein (AtPUCP1) expressed in Escherichia coli. FEBS Lett 505:240–244
Borner GHH, Lilley KS, Stevens TJ, Dupree P (2003) Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol 132:568–577
Bourdais G, Burdiak P, Gauthier A, Nitsch L, Salojärvi J, Rayapuram C, Idänheimo N, Hunter K, Kimura S, Merilo E, Vaattovaara A, Oracz K, Kaufholdt D, Pallon A, Anggoro DT, Glów D, Lowe J, Zhou J, Mohammadi O, Puukko T, Albert A, Lang H, Ernst D, Kollist H, Brosché M, Durner J, Borst JW, Collinge DB, Karpiński S, Lyngkjær MF, Robatzek S, Wrzaczek M, Kangasjärvi J (2015) Large-scale phenomics identifies primary and fine-tuning roles for CRKs in responses related to oxidative stress. PLoS Genet 11:e1005373
Bruinsma J (1961) A comment on the spectrophotometric determination of chlorophyll. Biochim Biophys Acta 52:578–582
Burdiak P, Rusaczonek A, Witon D, Glow D, Karpinski S (2015) Cysteine-rich receptor-like kinase CRK5 as a regulator of growth, development, and ultraviolet radiation responses in Arabidopsis thaliana. J Exp Bot 66:3325–3337
Caselato-Sousa VM, Amaya-Farfán J (2012) State of knowledge on amaranth grain: a comprehensive review. J Food Sci 77:R93–R104
Chen T, Cui P, Chen H, Ali S, Zhang S, Xiong L (2013) A KH-domain RNA-binding protein interacts with FIERY2/CTD phosphatase-like 1 and splicing factors and is important for pre-mRNA splicing in Arabidopsis. PLoS Genet 9:e1003875
Chen YH, Shen HL, Hsu PJ, Hwang SG, Cheng WH (2014) N-Acetylglucosamine-1-P uridylyltransferase 1 and 2 are required for gametogenesis and embryo development in Arabidopsis thaliana. Plant Cell Physiol 55:1977–1993
Cheng SF, Huang YP, Wu ZR, Hu CC, Hsu YH, Tsai CH (2010) Identification of differentially expressed genes induced by Bamboo mosaic virus infection in Nicotiana benthamiana by cDNA-amplified fragment length polymorphism. BMC Plant Biol 10:286
Clouse JW, Adhikary D, Page JT, Ramaraj T, Deyholos MK, Udall JA, Fairbanks DJ, Jellen EN, Maughan PJ (2016) The amaranth genome: genome, transcriptome, and physical map assembly. Plant Genome 9:1–14
Colombo PM, Rascio N (1977) Ruthenium red staining for electron microscopy of plant material. J Ultrastruct Res 60:135–139
Cook NP, Archer CM, Fawver JN, Schall HE, Rodriguez-Rivera J, Dineley KT, Martí AA, Murray JV (2012) Ruthenium red colorimetric and birefringent staining of amyloid-β aggregates in vitro and in tg2576 mice. ACS Chem Neurosci 4:379–384
Des Marais DL, McKay JK, Richards JH, Sen S, Wayne T, Juenger TE (2012) Physiological genomics of response to soil drying in diverse Arabidopsis accessions. Plant Cell 24:893–914
Del Bem LEV, Vincentz MGA (2010) Evolution of xyloglucan-related genes in green plants. BMC Evol Biol 10:341
Del Vecchio HA, Ying S, Park J, Knowles VL, Kanno S, Tanoi K, She YM, Plaxton WC (2014) The cell wall-targeted purple acid phosphatase AtPAP25 is critical for acclimation of Arabidopsis thaliana to nutritional phosphorus deprivation. Plant J 80:569–581
Délano-Frier JP, Avilés-Arnaut H, Casarrubias-Castillo K, Casique-Arroyo G, Castrillón-Arbeláez PA, Herrera-Estrella L, Massange-Sánchez J, Martínez-Gallardo NA, Parra-Cota FI, Vargas-Ortiz E, Estrada-Hernández MG (2011) Transcriptomic analysis of grain amaranth (Amaranthus hypochondriacus) using 454 pyrosequencing: comparison with A. tuberculatus, expression profiling in stems and in response to biotic and abiotic stress. BMC Genom 12:363
Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang JM, Taly JF, Notredame C (2011) T-coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 39:W13–W17
Diaz M, Sanchez-Barrena MJ, Gonzalez-Rubio JM, Rodriguez L, Fernandez D, Antoni R, Yunta C, Belda-Palazon B, Gonzalez-Guzman M, Peirats-Llobet M, Menendez M, Boskovic J, Marquez JA, Rodriguez PL, Albert A (2016) Calcium-dependent oligomerization of CAR proteins at cell membrane modulates ABA signaling. Proc Natl Acad Sci USA 113:396–405
Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230
Gao Y, Badejo AA, Sawa Y, Ishikawa T (2012) Analysis of two l-galactono-1, 4-lactone-responsive genes with complementary expression during the development of Arabidopsis thaliana. Plant Cell Physiol 53:592–601
García-Armenta E, Téllez-Medina DI, Sánchez-Segura L, Alamilla-Beltrán L, Hernández-Sánchez H, Gutiérrez-López GF (2016) Multifractal breakage pattern of tortilla chips as related to moisture content. J Food Eng 168:96–104
Guzmán P (2012) The prolific ATL family of RING-H2 ubiquitin ligases. Plant Signal Behav 7:1014–1021
Hartmann L, Pedrotti L, Weiste C, Fekete A, Schierstaedt J, Göttler J, Kempa S, Krischke M, Dietrich K, Mueller MJ, Vicente-Carbajosa J, Hanson J, Dröge-Laser W (2015) Crosstalk between two bZIP signaling pathways orchestrates salt-induced metabolic reprogramming in Arabidopsis roots. Plant Cell 27:2244–2260
Hondo D, Hase S, Kanayama Y, Yoshikawa N, Takenaka S, Takahashi H (2007) The LeATL6-associated ubiquitin/proteasome system may contribute to fungal elicitor-activated defense response via the jasmonic acid-dependent signaling pathway in tomato. Mol Plant Microbe Interact 20:72–81
Huizinga DH, Omosegbon O, Omery B, Crowell DN (2008) Isoprenylcysteine methylation and demethylation regulate abscisic acid signaling in Arabidopsis. Plant Cell 20:2714–2728
Husbands A, Bell EM, Shuai B, Smith HM, Springer PS (2007) LATERAL ORGAN BOUNDARIES defines a new family of DNA-binding transcription factors and can interact with specific bHLH proteins. Nucleic Acids Res 35:6663–6671
Irshad M, Canut H, Borderies G, Pont-Lezica R, Jamet E (2008) A new picture of cell wall protein dynamics in elongating cells of Arabidopsis thaliana: confirmed actors and newcomers. BMC Plant Biol 8:94
Jin J, Shi J, Liu B, Liu Y, Huang Y, Yu Y, Dong A (2015) MORF-RELATED GENE702, a reader protein of trimethylated histone H3 lysine 4 and histone H3 lysine 36, is involved in brassinosteroid-regulated growth and flowering time control in rice. Plant Physiol 168:1275–1285
Kaida R, Serada S, Norioka N, Norioka S, Neumetzler L, Pauly M, Sampedro J, Zarra I, Hayashi T, Kaneko TS (2010) Potential role for purple acid phosphatase in the dephosphorylation of wall proteins in tobacco cells. Plant Physiol 153:603–610
Kim JM, Sasaki T, Ueda M, Sako K, Seki M (2015) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6:114
Klavons JA, Bennett RD (1986) Determination of methanol using alcohol oxidase and its application to methyl ester content of pectins. J Agric Food Chem 34:597–599
Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141
Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5:305–315
Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 4:112–166
Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320
Lee JH, Kim YC, Choi D, Park JM (2013) Identification of novel pepper genes involved in Bax- or INF1-mediated cell death responses by high-throughput virus-induced gene silencing. Int J Mol Sci 14:22782–22795
Li DX, Chen WQ, Xu ZH, Bai SN (2015) HDA6-defective mutants show increased expression and acetylation of ETC1 and GL2 with small but significant effects on root epidermis cellular pattern. Plant Physiol 168:1448–1458
Lin Z, Ho CW, Grierson D (2009) AtTRP1 encodes a novel TPR protein that interacts with the ethylene receptor ERS1 and modulates development in Arabidopsis. J Exp Bot 60:3697–3714
Liu Y, Douglas CJ (2015) A role for OVATE FAMILY PROTEIN1 (OFP1) and OFP4 in a BLH6-KNAT7 multi-protein complex regulating secondary cell wall formation in Arabidopsis thaliana. Plant Signal Behav 10:e1033126
Liu F, Zhang X, Lu C, Zeng X, Li Y, Fu D, Wu G (2015) Nonspecific lipid transfer proteins in plants: presenting new advances and an integrated functional analysis. J Exp Bot 66:5663–5681
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408
Long R, Yang Q, Kang J, Zhang T, Wang H, Li M, Zhang Z (2013) Overexpression of a novel salt stress-induced glycine-rich protein gene from alfalfa causes salt and ABA sensitivity in Arabidopsis. Plant Cell Rep 32:1289–1298
Mandelbrot BB (1983) The fractal geometry of nature, 3rd edn. W.H. Freeman and Company, New York, pp 310–318
Mangeon A, Lin WC, Springer PS (2012) Functional divergence in the Arabidopsis LOB-domain gene family. Plant Signal Behav 7:1544–1547
Martinez-Trujillo M, Limones-Briones V, Cabrera-Ponce JL, Herrera-Estrella L (2004) Improving transformation efficiency of Arabidopsis thaliana by modifying the floral dip method. Plant Mol Biol Rep 22:63–70
Massange-Sanchez JA, Palmeros-Suarez PA, Martinez-Gallardo NA, Castrillon-Arbeláez PA, Avilés-Arnaut H, Alatorre-Cobos F, Tiessen A, Délano-Frier JP (2015) The novel and taxonomically restricted Ah24 gene from grain amaranth (Amaranthus hypochondriacus) has a dual role in development and defense. Front Plant Sci 6:602
Massange-Sánchez JA, Palmeros-Suaárez PA, Espitia-Rangel E, Rodríguez-Arévalo I, Sánchez-Segura L, Martínez-Gallardo NA, Alatorre-Cobos F, Tiessen A, Délano-Frier JP (2016) Overexpression of grain amaranth (Amaranthus hypochondriacus) AhERF or AhDOF transcription factors in Arabidopsis thaliana increases water deficit- and salt-stress tolerance, respectively, via contrasting stress-amelioration mechanisms. PLoS One 11:e0164280
McCann MC, Carpita NC (2008) Designing the deconstruction of plant cell walls. Curr Opin Plant Biol 11:314–320
Mewalal R, Mizrachi E, Mansfield SD, Myburg A (2014) Cell wall-related proteins of unknown function: missing links in plant cell wall development. Plant Cell Physiol 55:1031–1043
Miyakawa T, Hatano K, Miyauchi Y, Suwa Y, Sawano Y, Tonokura M (2014) A secreted protein with plant-specific cysteine-rich motif functions as a mannose-binding lectin that exhibits antifungal activity. Plant Physiol 166:766–778
Niemann MCE, Bartrina I, Ashikov A, Weber H, Novák O, Spíchal L, Strnad M, Strasser R, Bakker H, Schmülling T, Werner T (2015) Arabidopsis ROCK1 transports UDP-GlcNAc/UDP-GalNAc and regulates ER protein quality control and cytokinin activity. Proc Natl Acad Sci USA 112:291–296
Nozaki M, Sugiyama M, Duan J, Uematsu H, Genda T, Sato Y (2012) A missense mutation in the glucosamine-6-phosphate N-acetyltransferase- encoding gene causes temperature-dependent growth defects and ectopic lignin deposition in Arabidopsis. Plant Cell 24:3366–3379
Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604
Palmeros-Suárez PA, Massange-Sánchez JA, Martínez-Gallardo NA, Montero-Vargas JM, Gómez-Leyva JF, Délano-Frier JP (2015) The overexpression of an Amaranthus hypochondriacus NF-YC gene modifies growth and confers water deficit stress resistance in Arabidopsis. Plant Sci 240:25–40
Parvaiz A, Satyawati S (2008) Salt stress and phyto-biochemical responses of plants—a review. Plant Soil Environ 54:89–99
Pittman JK (2012) Multiple transport pathways for mediating intra-cellular pH homeostasis: the contribution of H+/ion exchangers. Front Plant Sci 3:11
Qin Y, Wang M, Tian Y, He W, Han L, Xia G (2012) Over-expression of TaMYB33 encoding a novel wheat MYB transcription factor increases salt and drought tolerance in Arabidopsis. Mol Biol Rep 39:7183–7192
Ripoll JJ, Rodríguez-Cazorla E, González-Reig S, Andújar A, Alonso-Cantabrana H, Perez-Amador MA, Carbonell J, Martínez-Laborda A, Vera A (2006) PEPPER, a novel K-homology domain gene, regulates vegetative and gynoecium development in Arabidopsis. Dev Biol 289:346–359
Rojas-González JA, Soto-Súarez M, García-Díaz Á, Romero-Puertas MC, Sandalio LM, Mérida Á, Thormählen I, Geigenberger P, Serrato AJ, Sahrawy M (2015) Disruption of both chloroplastic and cytosolic FBPase genes results in a dwarf phenotype and important starch and metabolite changes in Arabidopsis thaliana. J Exp Bot 66:2673–2689
Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R, Menzel D, Salinas J, Mancuso S, Valpuesta V, Baluska F, Botella MA (2008) Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20:3374–3388
Sharma M, Pandey GK (2016) Expansion and function of repeat domain proteins during stress and development in plants. Front Plant Sci 6:1218
Shin K, Lee S, Song WY, Lee RA, Lee I, Ha K, Koo JC, Park SK, Nam HG, Lee Y, Soh MS (2015) Genetic identification of ACC-RESISTANT2 reveals involvement of LYSINE HISTIDINE TRANSPORTER1 in the uptake of 1-aminocyclopropane-1-carboxylic acid in Arabidopsis thaliana. Plant Cell Physiol 56:572–582
Soeda Y, Konings MCJM, Vorst O, van Houwelingen AMML, Stoopen GM, Maliepaard CA, Kodde J, Bino RJ, Groot SPC, van der Geest A (2005) Gene expression programs during Brassica oleracea seed maturation, osmopriming, and germination are indicators of progression of the germination process and the stress tolerance level. Plant Physiol 137:354–368
Sreenivasulu N, Usadel B, Winter A, Radchuk V, Scholz U, Stein N, Weschke W, Strickert M, Close TJ, Stitt M, Graner A, Wobus U (2008) Barley grain maturation and germination; metabolic pathway and regulatory network commonalities and differences highlighted by new MapMan/PageMan profiling tools. Plant Physiol 146:1738–1758
Stael S, Wurzinger B, Mair A, Mehlmer N, Vothknecht UC, Teige M (2012) Plant organellar calcium signalling: an emerging field. J Exp Bot 63:1525–1542
Takano J, Wada M, Ludewig U, Schaaf G, von Wiren N, Fujiwara T (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18:1498–1509
Tanveer T, Shaheen K, Parveen S, Kazi AG, Ahmad P (2014) Plant secretomics: identification, isolation, and biological significance under environmental stress. Plant Signal Behav 9:e29426
Tarte V, Seok HY, Woo DH, Le D, Tran H, Baik JW, In Soon Kang IS, Sun-Young Lee SY, Chung T, Moon YH (2015) Arabidopsis Qc-SNARE gene AtSFT12 is involved in salinity and osmotic stress responses and Na+ accumulation in vacuoles. Plant Cell Rep 34:1127–1138
Tavares B, Domingos P, Dias PN, Feijó JA, Bicho A (2011) The essential role of anionic transport in plant cells: the pollen tube as a case study. J Exp Bot 62:2273–2298
Trono D, Laus MN, Soccio M, Alfarano M, Pastore D (2015) Modulation of potassium channel activity in the balance of ROS and ATP Production by Durum wheat mitochondria-an amazing defense tool against hyperosmotic stress. Front Plant Sci 6:1072
Vázquez-Lobo A, Roujol D, Zúñiga-Sánchez E, Albenne C, Piñero D, de Buen AG, Jamet E (2012) The highly conserved spermatophyte cell wall DUF642 protein family: phylogeny and first evidence of interaction with cell wall polysaccharides in vitro. Mol Phylogenet Evol 63:510–520
Vilches-Barro A, Maizel A (2015) Talking through walls: mechanisms of lateral root emergence in Arabidopsis thaliana. Curr Opin Plant Sci 23:31–38
Wang Z, Wang Y, Hong X, Hu D, Liu C, Yang J, Li Y, Huang Y, Feng Y, Gong H, Li Y, Fang G, Tang H, Li Y (2015) Functional inactivation of UDP-N-acetylglucosamine pyrophosphorylase 1 (UAP1) induces early leaf senescence and defence responses in rice. J Exp Bot 66:973–987
Wellmer F, Riechmann JL, Alves-Ferreira M, Meyerowitz EM (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16:1314–1326
Wiese J (2014) Propionate metabolism in yeast and plants. Doctoral Dissertation. Heinrich-Heine University Düsseldorf, Düsseldorf, Germany
Yang T, Echols M, Martin A, Bar-Peled M (2010) Identification and characterization of a strict and a promiscuous N-acetylglucosamine-1-P uridylytransferase in Arabidopsis. Biochem J 430:275–284
Yao X, Feng H, Yu Y, Dong A, Shen W-H (2013) SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growth and development. PLoS ONE 8:e56537
Zhang Y, Behrens I, Zimmermann R, Ludwig Y, Hey S, Hochholdinger F (2015) LATERAL ROOT PRIMORDIA 1 of maize acts as a transcriptional activator in auxin signalling downstream of the Aux/IAA gene rootless with undetectable meristem 1. J Exp Bot 66:3855–3863
Zúñiga-Sánchez E, Gamboa-de Buen A (2012) The two DUF642 At5g11420 and At4g32460-encoded proteins interact in vitro with the AtPME3 catalytic domain. In: Cai J (ed) Protein interactions, Book 1. InTech, Rijeka, pp 119–142
Zúñiga-Sánchez E, Soriano D, Martínez-Barajas E, Orozco-Segovia A, Gamboa-deBuen A (2014) BIIDXI, the At4g32460 DUF642 gene, is involved in pectin methylesterase regulation during Arabidopsis thaliana seed germination and plant development. BMC Plant Biol 14:338
Acknowledgements
Acknowledgements are due to The National Council for Science and Technology (CONACyT, México; Grant No. 156912, to JPDF), to the European Commission 6th Framework Programme, AMARANTH: FUTURE FOOD (Contract No. 032263, to JPDF), to México Tierra de Amaranto A. C. and to The Deborah Presser-Velder Foundation for financial support. JMS and PAPS were supported by postgraduate scholarships (Codes Nos. 234771 and 232807, respectively), granted by CONACyT, México.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Palmeros-Suárez, P.A., Massange-Sánchez, J.A., Sánchez-Segura, L. et al. AhDGR2, an amaranth abiotic stress-induced DUF642 protein gene, modifies cell wall structure and composition and causes salt and ABA hyper-sensibility in transgenic Arabidopsis. Planta 245, 623–640 (2017). https://doi.org/10.1007/s00425-016-2635-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-016-2635-y