Volume 6, Issue 6, December 2018, Page: 185-197
Overexpression of Transcription Factor WRKY76 in Rice Leaves Leads to Increased Photosynthesis and Plant Yield
Alanna Jane Oiestad, Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, USA
Hannah Margaret Turner, Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, USA
Brian Stuart Beecher, USDA-GIPSA Technology and Science Division, Kansas City, USA
John Munson Martin, Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, USA
Michael Joseph Giroux, Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, USA
Received: Nov. 12, 2018;       Accepted: Dec. 3, 2018;       Published: Jan. 10, 2019
DOI: 10.11648/j.jps.20180606.11      View  231      Downloads  72
Abstract
The rate of leaf starch biosynthesis impacts overall plant growth and yield. Overexpression of ADP-glucose pyrophosphorylase (AGPase), the rate limiting enzyme in the starch pathway, has led to increased plant growth in multiple species. Our goal here was to identify and test transcription factors that themselves upregulate starch biosynthetic genes. To accomplish this objective, we examined rice genes upregulated in response to overexpression of leaf AGPase, and identified the transcription factor (TF) WRKY76 as a potential regulator of the rice leaf starch biosynthesis pathway. Overexpression of WRKY76 in rice (Oyrza sativa) leaves led to a 27% increase in plant growth and seed yield. The enhanced productivity phenotype in rice overexpressing WRKY76 was associated with a 40% increase in leaf starch levels at one month after planting and at anthesis. This was accompanied by a 16% increase in photosynthetic rate and 20% increase in net carbon metabolism, indicating that WRKY76 positively regulates leaf starch biosynthesis and carbon metabolism. Interestingly, increased expression of WRKY76 led to changes in expression of other WRKY TFs, indicating that the mechanism by which WRKY76 regulates starch biosynthesis involves a complicated regulatory network. This research indicates that WRKY76 directly increases expression of genes involved in leaf starch biosynthesis.
Keywords
ADP-glucose Pyrophosphorylase (AGPase), Photosynthesis, Starch, Transcription Factor (TF), WRKY, Yield
To cite this article
Alanna Jane Oiestad, Hannah Margaret Turner, Brian Stuart Beecher, John Munson Martin, Michael Joseph Giroux, Overexpression of Transcription Factor WRKY76 in Rice Leaves Leads to Increased Photosynthesis and Plant Yield, Journal of Plant Sciences. Vol. 6, No. 6, 2018, pp. 185-197. doi: 10.11648/j.jps.20180606.11
Copyright
Copyright © 2018 Authors retain the copyright of this article.
This article is an open access article distributed under the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Reference
[1]
G. J. MacNeill, S. Mehrpouyan, M. A. A. Minow, J. A. Patterson, I. J. Tetlow, M. J. Emes, Starch as a source, starch as a sink: the bifunctional role of starch in carbon allocation, J. Exp. Bot. 68 (2017) 4433-4453.
[2]
A. Tuncel, T. W. Okita, Improving starch yield in cereals by over-expression of ADPglucose pyrophosphorylase: expectations and unanticipated outcomes, Plant Sci. 211 (2013) 52-60.
[3]
J. Espada, Enzymic synthesis of adenosine diphosphate glucose from glucose 1-phosphate and adenosine triphosphate, J. Biol. Chem. 237 (1992) 3557-3581.
[4]
A. J. Schlosser, J. M. Martin, L. C. Hannah, M. J. Giroux, The maize leaf starch mutation agps-m1 has diminished field growth and productivity, Crop Sci. 52 (2012) 700-706.
[5]
T. W. Greene, L. C. Hannah, Enhanced stability of maize endosperm ADP-glucose pyrophosphorylase is gained through mutants that alter subunit interactions, Proc. Natl. Acad. Sci. USA 95 (1998) 13342-13347.
[6]
S.-M. Lee, T.-H. Ryu, S.-I. Kim, T. Okita, D. Kim, Kinetic and regulatory properties of plant ADP-glucose pyrophosphorylase genetically modified by heterologous expression of potato upreg mutants in vitro and in vivo, Plant Cell Tiss. Org. 96 (2009) 161-170.
[7]
K. Gibson, J. S. Park, Y. Nagai, S. K. Hwang, Y. C. Cho, K. H. Roh, S. M. Lee, D. H. Kim, S. B. Choi, H. Ito, G. E. Edwards, T. W. Okita, Exploiting leaf starch synthesis as a transient sink to elevate photosynthesis, plant productivity and yields, Plant Sci. 181 (2011) 275-281.
[8]
A. J. Schlosser, J. M. Martin, B. Beecher, M. J. Giroux, Enhanced rice growth is conferred by increased leaf ADP-glucose pyrophosphorylase activity, J. Plant Physiol. Pathol. 2 (2014) 4.
[9]
A. J. Oiestad, J. M. Martin, M. J. Giroux, Overexpression of AGPase in source and sink tissue, Funct. Plant Biol. 43 (2016) 1194-1204.
[10]
F. D. Meyer, L. E. Talbert, J. M. Martin, S. P. Lanning, T. W. Greene, M. J. Giroux, Field evaluation of transgenic wheat expressing a modified ADP-glucose pyrophosphorylase large subunit, Crop Sci. 47 (2007) 336-342.
[11]
F. Spitz, E. E. M. Furlong, Transcription factors: from enhancer binding to developmental control, Nat. Rev. Genet. 13 (2012) 613-626.
[12]
C. Schluttenhofer, L. Yuan, Regulation of specialized metabolism by WRKY transcription factors, Plant Physiol. 167 (2015) 295-306.
[13]
J. C. Wang, H. Xu, Y. Zhu, Q. Q. Liu, X. L. Cai, OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm, J. Exp. Bot. 64 (2013) 3453-3466.
[14]
F. F. Fu, H. W. Xue, Coexpression analysis identifies Rice Starch Regulator 1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator, Plant Physiol. 154 (2010) 927-938.
[15]
M. M. R. Ambavaram, S. Basu, A. Krishnan, V. Ramegowda, U. Batlang, L. Rahman, N. Baisakh, A. Pereira, Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress, Nat. Commun. 5 (2014) 5302.
[16]
T. Nagata, H. Hara, K. Saitou, A. Kobashi, K. Kojima, T. Yuasa, O. Ueno, Activation of ADP-glucose pyrophosphorylase gene promoters by a WRKY transcription factor, AtWRKY20, in Arabidopsis thaliana L. and Sweet Potato (Ipomoea batatas Lam.), Plant Prod. Sci. 15 (2012) 10-18.
[17]
M. M. Paz, H. Shou, Z. Guo, Z. Zhang, A. K. Banerjee, K. Wang, Assessment of conditions affecting Agrobacterium-mediated soybean transformation using the cotyledonary node explant, Euphytica 136 (2004) 167-179.
[18]
P. Hajdukiewicz, Z. Svab, P. Maliga, The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation, Plant Mol. Biol. 25 (1994) 989-994.
[19]
J. T. Odell, F. Nagy, N.-H. Chua, Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter, Nature 313 (1985) 810-812.
[20]
J. C. Carrington, D. D. Freed, Cap-independent enhancement of translation by a plant potyvirus 5' nontranslated region, J. Virol. 64 (1990) 1590-1597.
[21]
H. S. Mason, D. B. DeWald, J. E. Mullet, Identification of a methyl jasmonate-responsive domain in the soybean vspB promoter, Plant Cell 5 (1993) 241-251.
[22]
G. C. Allen, S. Spiker, W. F. Thompson, Use of matrix attachment regions (MARs) to minimize transgene silencing. Plant Mol. Biol. 43 (2000) 361-376.
[23]
S. Toki, Rapid and efficient Agrobacterium-mediated transformation in rice. Plant Mol Biol Rep 15 (1997) 16-21.
[24]
B.-R. Kim, Y.-H. Nam, S.-U. Kim, S.-I. Kim, Y.-J. Chang, Normalization of reverse transcription quantitative-PCR with housekeeping genes in rice, Biotechnol. Lett. 25 (2003) 1869-1872.
[25]
H. Xu, Y. Gao, J. Wang, Transcriptomic analysis of rice (Oryza sativa) developing embryos using the RNA-Seq technique, PLOS One 7 (2012) e30646.
[26]
A. Mortazavi, B. A. Williams, K. McCue, L. Schaeffer, B. Wold, Mapping and quantifying mammalian transcriptomes by RNA-Seq, Nat. Methods 5 (2008) 621-628.
[27]
D. W. Huang, B. T. Sherman, R. A. Lempicki, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources, Nat. Protoc. 4 (2009) 44-57.
[28]
A. M. Smith, S. C. Zeeman, Quantification of starch in plant tissues, Nat. Protoc. 1 (2006) 1342-1345.
[29]
S. Rösti, H. Rudi, K. Rudi, H.-G. Opsahl-Sorteberg, B. Fahy, K. Denyer, The gene encoding the cytosolic small subunit of ADP-glucose pyrophosphorylase in barley endosperm also encodes the major plastidial small subunit in the leaves, J. Exp. Bot. 57 (2006) 3619-3626.
[30]
M. A. Schmidt, W. B. Barbazuk, M. Sandford, G. May, Z. Song, W. Zhou, B. J. Nikolau, E. M. Herman, Silencing of soybean seed storage proteins results in a rebalanced protein composition preserving seed protein content without major collateral changes in the metabolome and transcriptome, Plant Physiol. 156 (2011) 330-345.
[31]
O. Fiehn, G. Wohlgemuth, M. Scholz, T. Kind, D. Y. Lee, Y. Lu, S. Moon, B. Nikolau, Quality control for plant metabolomics: reporting MSI‐compliant studies, Plant J. 53 (2008) 691-704.
[32]
E. D. Smidansky, F D. Meyer, B. Blakeslee, T. E. Weglarz, T. W. Greene, M. J. Giroux, Expression of a modified ADP-glucose pyrophosphorylase large subunit in wheat seeds stimulates photosynthesis and carbon metabolism, Planta 225 (2007) 965-976.
[33]
E. D. Smidansky, J. M. Martin, L. C. Hannah, A. M. Fischer, M. J. Giroux, Seed yield and plant biomass increases in rice are conferred by deregulation of endosperm ADP-glucose pyrophosphorylase, Planta 216 (2003) 656-664.
[34]
R. Eddy, D. T. Hahn, Optimizing greenhouse rice production: what is the best fertilization schedule? Purdue Methods for Rice Growth, paper 4. Purdue e-Pubs (2004).
[35]
K. Wu, Z. Guo, H. Wang, J. Li, The WRKY family of transcription factors in rice and Arabidopsis and their origins, DNA Res. 12 (2005) 9-26.
[36]
Y. Chi, Y. Yang, Y. Zhou, J. Zhou, B. Fan, J. Q. Yu, Z. Chen, Protein-protein interactions in the regulation of WRKY transcription factors, Mol. Plant 6 (2013) 287-300.
[37]
T. L. Hennessey, C. B. Field, Circadian rhythms in photosynthesis: oscillations in carbon assimilation and stomatal conductance under constant conditions, Plant Physiol. 96 (1991) 831-836.
[38]
E. Mangelsen, J. Kilian, K. W. Berendzen, Ü. H. Kolukisaoglu, K. Harter, C. Jansson, D. Wanke, Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare) WRKY transcription factor family reveals putatively retained functions between monocots and dicots, BMC Genomics 9 (2008) 194.
[39]
S. Berri, P. Abbruscato, O. Faivre-Rampant, A. C. Brasileiro, I. Fumasoni, K. Satoh, S. Kikuchi, L. Mizzi, P. Morandini, M. E. Pè, Characterization of WRKY co-regulatory networks in rice and Arabidopsis, BMC Plant Biol. 9 (2009) 120.
[40]
S. Proietti, L. Bertini, S. Van der Ent, A. Leon-Reyes, C. Pieterse, M. Tucci, C. Caporale, C. Caruso, Cross activity of orthologous WRKY transcription factors in wheat and Arabidopsis. J. Exp. Bot. 62 (2011) 1975-1990.
[41]
N. Yokotani, Y. Sato, S. Tanabe, T. Chujo, T. Shimizu, K. Okada, H. Yamane, M. Shimono, S. Sugano, H. Takatsuji, WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance, J. Exp. Bot. 64 (2013) 5085-5097.
[42]
C. A. Griffiths, M. J. Paul, C. H. Foyer, Metabolite transport and associated sugar signaling systems underpinning source/sink interactions, Biochim. Biophys. Acta 1857 (2016) 1715-1725.
[43]
T. Eulgem, P. J. Rushton, S. Robatzek, I. E. Somssich, The WRKY superfamily of plant transcription factors, Trends Plant Sci. 5 (2000) 199-206.
[44]
Z. Xie, Z. L. Zhang, X. Zou, J. Huang, P. Ruas, D. Thompson, Q. J. Shen, Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells, Plant Physiol. 137 (2005) 176-189.
[45]
C. A. Ross, Y. Liu, Q. J. Shen, The WRKY gene family in rice (Oryza sativa), J. Int. Plant Biol. 49 (2007) 827-842.
[46]
X. Xu, C. Chen, B. Fan, Z. Chen, Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors, Plant Cell 18 (2006) 1310-1326.
[47]
X. Liu, X. Bai, X. Wang, C. Chu, OsWRKY71, a rice transcription factor, is involved in rice defense response, J. Plant Physiol. 164 (2007) 969-979.
[48]
Y. Shang, L. Yan, Z.-Q. Liu, Z. Cao, C. Mei, Q. Xin, F.-Q. Wu, X.-F. Wang, S.-Y. Du, T. Jiang, The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition, Plant Cell 22 (2010) 1909-1935.
[49]
H. Sakai, H. Mizuno, Y. Kawahara, H. Wakimoto, H. Ikawa, H. Kwahigashi, H. Kanomori, T. Matsumoto, T. Itoh, B. S. Gaut, Retrogenes in rice (Oryza sativa L. ssp. japonica) exhibit correlated expression with their source genes, Genome Biol. Evol. 3 (2011) 1357-1368.
[50]
R. M. Davidson, M. Gowda, G. Moghe, H. Lin, B. Vailancourt, S.-H. Shiu, N. Jang, C. R. Buell, Comparative transcriptomics of three Poacee species reveal patterns of gene expression, Plant J. 71 (2012) 492-502.
[51]
S. N. Anderson, C. S. Johnson, D. S. Jones, L. J. Conrad, X. Gou, S. D. Russel, Transcriptomes of isolated Oryza sativa gametes characterized by deep sequencing: evidence for distinct sex-dependent chromatin and epigenetic states before fertilization, Plant J. 76 (2013) 729-741.
[52]
Y.-C. Zhang, J.-Y. Liao, Z.-Y. Li, Y. Yu, J.-P. Zhang, Z.-F. Li, L.-H. Qu, W.-S. Shu, Y.-Q. Chen, Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice, Genome Biol. 15 (2014) 512.
[53]
U. Zentgraf, T. Laun, Y. Miao, The complex regulation of WRKY53 during leaf senescence of Arabidopsis thaliana, Eur. J. Cell Biol. 89 (2010) 133-137.
[54]
A. Banerjee, A. Roychoudhury, WRKY proteins: signaling and regulation of expression during abiotic stress responses, Sci. World J. 2015 (2015) 807560.
[55]
X. Peng, X. Tang, P. Zhou, X. Deng, H. Wang, Z. Guo, Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice. Planta 236 (2012) 1485-1498.
[56]
Z.-L. Zhang, Z. Xie, X. Zou, J. Casaretto, T. H.-D. Ho, Q. J. Shen, A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol. 134 (2004) 1500-1513.
[57]
M. Stitt, D. Schulze, Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology, Plant Cell Environ. 17 (1994) 465-487.
[58]
J. Lopez-Bucio, M. F. Nieto-Jacobo, V. V. Ramirez-Rodriguez, L. Herrera-Estrella, Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils, Plant Sci. 160 (2000) 1-13.
[59]
J. Wang, Q. Shen, Roles of organic acid metabolism in plant adaptation to nutrient deficiency and aluminum toxicity stress, J. Appl. Ecol. 11 (2006) 2210-2216.
[60]
J. Jiang, S. Ma, N. Ye, M. Jiang, J. Cao, J. Zhang, WRKY transcription factors in plant responses to stresses, J. Integr. Plant Biol. 59 (2017) 86-101.
[61]
T. Pawson, J. D. Scott, Protein phosphorylation in signaling – 50 years and counting, Trends Biochem. Sci. 30 (2005) 286-290.
[62]
T. Hunter, Tyrosine phosphorylation: thirty years and counting, Curr. Opin. Cell Biol. 21 (2009) 140-146.
[63]
L. J. Meyer, J. Gao, D. Xu, J. J. Thelen, Phosphoproteomic analysis of seed maturation in Arabidopsis, rapeseed, and soybean, Plant Physiol. 159 (2012) 517-528.
[64]
G. X. Chen, J. W. Zhou, Y. L. Liu, X. B. Lu, C. X. Han, W. Y. Zhang, Y. H. Xu, Y. M. Yan, Biosynthesis and regulation of wheat amylose and amylopectin from proteomic and phosphoproteomic characterization of granule-binding proteins, Sci. Reports 6 (2016) 33111.
[65]
M. Bakshi, R. Oelmüller, WRKY transcription factors: Jack of many trades in plants, Plant Signal Behav. 9 (2014) e27700.
[66]
M. A. Parry, M. Reynolds, M. E. Salvucci, C. Raines, P. J. Andralojc, X. G. Zhu, G. D. Price, A. G. Condon, R. T, Furbank, Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency, J. Exp. Bot. 62 (2011) 453-467.
Browse journals by subject