OsWRKY21 and OsWRKY108 function redundantly to promote phosphate accumulation through maintaining the constitutive expression of OsPHT1;1 under phosphate‐replete conditions
Abstract
Summary Plant Phosphate Transporter 1 (PHT1) proteins, probably the only influx transporters for phosphate (Pi) uptake, are partially degraded on sufficient Pi levels to prevent excessive Pi accumulation. Therefore, the basal/constitutive expression level of PHT1 genes is vital for maintaining Pi uptake under Pi‐replete conditions. Rice ( Oryza sativa ) OsPHT1;1 is a unique gene as it is highly expressed and not responsive to Pi, however the mechanism for maintaining its basal/constitutive expression remains unknown. Using biochemical and genetic approaches, we identified and functionally characterised the transcription factors maintaining the basal/constitutive expression of OsPHT1;1 . OsWRKY21 and OsWRKY108 interact within the nucleus and both bind to the W‐box in the OsPHT1;1 promoter. Overexpression of OsWRKY21 or OsWRKY108 led to increased Pi accumulation, resulting from elevated expression of OsPHT1;1 . By contrast, oswrky21 oswrky108 double mutants showed decreased Pi accumulation and OsPHT1;1 expression in a Pi‐dependent manner. Moreover, similar to ospht1;1 mutants, plants expressing the OsWRKY21–SRDX fusion protein (a chimeric dominant suppressor) were impaired in Pi accumulation in Pi‐replete roots, accompanied by downregulation of OsPHT1;1 expression. Our findings demonstrated that rice WRKY transcription factors function redundantly to promote Pi uptake by activating OsPHT1;1 expression under Pi‐replete conditions, and represent a novelmore »
- Authors:
-
- State Key Laboratory of Crop Genetics and Germplasm Enhancement Nanjing Agricultural University Nanjing 210095 China
- State Key Laboratory of Crop Genetics and Germplasm Enhancement Nanjing Agricultural University Nanjing 210095 China, MOA Key Laboratory of Plant Nutrition and Fertilisation in Lower‐Middle Reaches of the Yangtze River Nanjing 210095 China, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilisation Nanjing 210095 China
- State Key Laboratory of Crop Genetics and Germplasm Enhancement Nanjing Agricultural University Nanjing 210095 China, MOA Key Laboratory of Plant Nutrition and Fertilisation in Lower‐Middle Reaches of the Yangtze River Nanjing 210095 China
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1671837
- Alternate Identifier(s):
- OSTI ID: 1781900
- Resource Type:
- Journal Article: Published Article
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Name: New Phytologist Journal Volume: 229 Journal Issue: 3; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Zhang, Jun, Gu, Mian, Liang, Ruisuhua, Shi, Xinyu, Chen, Lingling, Hu, Xu, Wang, Shichao, Dai, Xiaoli, Qu, Hongye, Li, Huanhuan, and Xu, Guohua. OsWRKY21 and OsWRKY108 function redundantly to promote phosphate accumulation through maintaining the constitutive expression of OsPHT1;1 under phosphate‐replete conditions. United Kingdom: N. p., 2020.
Web. doi:10.1111/nph.16931.
Zhang, Jun, Gu, Mian, Liang, Ruisuhua, Shi, Xinyu, Chen, Lingling, Hu, Xu, Wang, Shichao, Dai, Xiaoli, Qu, Hongye, Li, Huanhuan, & Xu, Guohua. OsWRKY21 and OsWRKY108 function redundantly to promote phosphate accumulation through maintaining the constitutive expression of OsPHT1;1 under phosphate‐replete conditions. United Kingdom. https://doi.org/10.1111/nph.16931
Zhang, Jun, Gu, Mian, Liang, Ruisuhua, Shi, Xinyu, Chen, Lingling, Hu, Xu, Wang, Shichao, Dai, Xiaoli, Qu, Hongye, Li, Huanhuan, and Xu, Guohua. 2020.
"OsWRKY21 and OsWRKY108 function redundantly to promote phosphate accumulation through maintaining the constitutive expression of OsPHT1;1 under phosphate‐replete conditions". United Kingdom. https://doi.org/10.1111/nph.16931.
@article{osti_1671837,
title = {OsWRKY21 and OsWRKY108 function redundantly to promote phosphate accumulation through maintaining the constitutive expression of OsPHT1;1 under phosphate‐replete conditions},
author = {Zhang, Jun and Gu, Mian and Liang, Ruisuhua and Shi, Xinyu and Chen, Lingling and Hu, Xu and Wang, Shichao and Dai, Xiaoli and Qu, Hongye and Li, Huanhuan and Xu, Guohua},
abstractNote = {Summary Plant Phosphate Transporter 1 (PHT1) proteins, probably the only influx transporters for phosphate (Pi) uptake, are partially degraded on sufficient Pi levels to prevent excessive Pi accumulation. Therefore, the basal/constitutive expression level of PHT1 genes is vital for maintaining Pi uptake under Pi‐replete conditions. Rice ( Oryza sativa ) OsPHT1;1 is a unique gene as it is highly expressed and not responsive to Pi, however the mechanism for maintaining its basal/constitutive expression remains unknown. Using biochemical and genetic approaches, we identified and functionally characterised the transcription factors maintaining the basal/constitutive expression of OsPHT1;1 . OsWRKY21 and OsWRKY108 interact within the nucleus and both bind to the W‐box in the OsPHT1;1 promoter. Overexpression of OsWRKY21 or OsWRKY108 led to increased Pi accumulation, resulting from elevated expression of OsPHT1;1 . By contrast, oswrky21 oswrky108 double mutants showed decreased Pi accumulation and OsPHT1;1 expression in a Pi‐dependent manner. Moreover, similar to ospht1;1 mutants, plants expressing the OsWRKY21–SRDX fusion protein (a chimeric dominant suppressor) were impaired in Pi accumulation in Pi‐replete roots, accompanied by downregulation of OsPHT1;1 expression. Our findings demonstrated that rice WRKY transcription factors function redundantly to promote Pi uptake by activating OsPHT1;1 expression under Pi‐replete conditions, and represent a novel pathway independent of the central Pi signalling system.},
doi = {10.1111/nph.16931},
url = {https://www.osti.gov/biblio/1671837},
journal = {New Phytologist},
issn = {0028-646X},
number = 3,
volume = 229,
place = {United Kingdom},
year = {Sat Oct 10 00:00:00 EDT 2020},
month = {Sat Oct 10 00:00:00 EDT 2020}
}
Works referenced in this record:
Phosphorus saturation and mobilization in two typical Chinese greenhouse vegetable soils
journal, April 2017
- Kalkhajeh, Yusef Kianpoor; Huang, Biao; Hu, Wenyou
- Chemosphere, Vol. 172
pho2 , a Phosphate Overaccumulator, Is Caused by a Nonsense Mutation in a MicroRNA399 Target Gene
journal, May 2006
- Aung, Kyaw; Lin, Shu-I; Wu, Chia-Chune
- Plant Physiology, Vol. 141, Issue 3
The paralogous R3 MYB proteins CAPRICE, TRIPTYCHON and ENHANCER OF TRY AND CPC1 play pleiotropic and partly non-redundant roles in the phosphate starvation response of Arabidopsis roots
journal, May 2015
- Chen, Chun-Ying; Schmidt, Wolfgang
- Journal of Experimental Botany, Vol. 66, Issue 15
OsMYB2P-1 , an R2R3 MYB Transcription Factor, Is Involved in the Regulation of Phosphate-Starvation Responses and Root Architecture in Rice
journal, March 2012
- Dai, Xiaoyan; Wang, Yuanyuan; Yang, An
- Plant Physiology, Vol. 159, Issue 1
A plant’s diet, surviving in a variable nutrient environment
journal, April 2020
- Oldroyd, Giles E. D.; Leyser, Ottoline
- Science, Vol. 368, Issue 6486
Spatio-Temporal Transcript Profiling of Rice Roots and Shoots in Response to Phosphate Starvation and Recovery
journal, November 2013
- Secco, D.; Jabnoune, M.; Walker, H.
- The Plant Cell, Vol. 25, Issue 11
WRKY42 Modulates Phosphate Homeostasis through Regulating Phosphate Translocation and Acquisition in Arabidopsis
journal, March 2015
- Su, Tong; Xu, Qian; Zhang, Fei-Cui
- Plant Physiology, Vol. 167, Issue 4
The Ubiquitin E3 Ligase PRU1 Regulates WRKY6 Degradation to Modulate Phosphate Homeostasis in Response to Low-Pi Stress in Arabidopsis
journal, March 2018
- Ye, Qing; Wang, Hui; Su, Tong
- The Plant Cell, Vol. 30, Issue 5
WRKY75 Transcription Factor Is a Modulator of Phosphate Acquisition and Root Development in Arabidopsis
journal, February 2007
- Devaiah, Ballachanda N.; Karthikeyan, Athikkattuvalasu S.; Raghothama, Kashchandra G.
- Plant Physiology, Vol. 143, Issue 4
Integrative Comparison of the Role of the PHOSPHATE RESPONSE1 Subfamily in Phosphate Signaling and Homeostasis in Rice
journal, June 2015
- Guo, Meina; Ruan, Wenyuan; Li, Changying
- Plant Physiology, Vol. 168, Issue 4
Characterization of the Rice PHO1 Gene Family Reveals a Key Role for OsPHO1;2 in Phosphate Homeostasis and the Evolution of a Distinct Clade in Dicotyledons
journal, January 2010
- Secco, David; Baumann, Arnaud; Poirier, Yves
- Plant Physiology, Vol. 152, Issue 3
Negative Regulation of Phosphate Starvation-Induced Genes
journal, December 2001
- Mukatira, Uthappa T.; Liu, Chunming; Varadarajan, Deepa K.
- Plant Physiology, Vol. 127, Issue 4
Overexpression of OsMYB4P, an R2R3-type MYB transcriptional activator, increases phosphate acquisition in rice
journal, July 2014
- Yang, Won Tae; Baek, Dongwon; Yun, Dae-Jin
- Plant Physiology and Biochemistry, Vol. 80
Reducing the Genetic Redundancy of Arabidopsis PHOSPHATE TRANSPORTER1 Transporters to Study Phosphate Uptake and Signaling
journal, February 2015
- Ayadi, Amal; David, Pascale; Arrighi, Jean-François
- Plant Physiology, Vol. 167, Issue 4
Coordination between zinc and phosphate homeostasis involves the transcription factor PHR1, the phosphate exporter PHO1, and its homologue PHO1;H3 in Arabidopsis
journal, January 2014
- Khan, Ghazanfar Abbas; Bouraine, Samir; Wege, Stefanie
- Journal of Experimental Botany, Vol. 65, Issue 3
Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation
journal, March 2009
- Ai, Penghui; Sun, Shubin; Zhao, Jianning
- The Plant Journal, Vol. 57, Issue 5
OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice: Regulation of Pi homeostasis in rice
journal, February 2010
- Liu, Fang; Wang, Zhiye; Ren, Hongyan
- The Plant Journal, Vol. 62, Issue 3
A Constitutive Expressed Phosphate Transporter, OsPht1;1, Modulates Phosphate Uptake and Translocation in Phosphate-Replete Rice
journal, May 2012
- Sun, Shubin; Gu, Mian; Cao, Yue
- Plant Physiology, Vol. 159, Issue 4
OsWRKY28 Regulates Phosphate and Arsenate Accumulation, Root System Architecture and Fertility in Rice
journal, September 2018
- Wang, Peitong; Xu, Xuan; Tang, Zhong
- Frontiers in Plant Science, Vol. 9
WRKY transcription factors
journal, May 2010
- Rushton, Paul J.; Somssich, Imre E.; Ringler, Patricia
- Trends in Plant Science, Vol. 15, Issue 5
The Rice CK2 Kinase Regulates Trafficking of Phosphate Transporters in Response to Phosphate Levels
journal, February 2015
- Chen, Jieyu; Wang, Yifeng; Wang, Fei
- The Plant Cell, Vol. 27, Issue 3
A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae
journal, August 2001
- Rubio, V.
- Genes & Development, Vol. 15, Issue 16
High-CO 2 /Hypoxia-Responsive Transcription Factors DkERF24 and DkWRKY1 Interact and Activate DkPDC2 Promoter
journal, March 2019
- Zhu, Qing-gang; Gong, Zi-yuan; Huang, Jingwen
- Plant Physiology, Vol. 180, Issue 1
The Phosphate Transporter Gene OsPht1;8 Is Involved in Phosphate Homeostasis in Rice
journal, April 2011
- Jia, Hongfang; Ren, Hongyan; Gu, Mian
- Plant Physiology, Vol. 156, Issue 3
A Reevaluation of the Role of Arabidopsis NRT1.1 in High-Affinity Nitrate Transport
journal, October 2013
- Glass, Anthony D. M.; Kotur, Zorica
- Plant Physiology, Vol. 163, Issue 3
Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis: Putative roles of Arabidopsis Pht1 genes
journal, August 2002
- Mudge, Stephen R.; Rae, Anne L.; Diatloff, Eugene
- The Plant Journal, Vol. 31, Issue 3
Upstream Open Reading Frame and Phosphate-Regulated Expression of Rice OsNLA1 Controls Phosphate Transport and Reproduction
journal, October 2019
- Yang, Shu-Yi; Lu, Wen-Chien; Ko, Swee-Suak
- Plant Physiology, Vol. 182, Issue 1
Node-Localized Transporters of Phosphorus Essential for Seed Development in Rice
journal, June 2020
- Che, Jing; Yamaji, Naoki; Miyaji, Takaaki
- Plant and Cell Physiology, Vol. 61, Issue 8
Phosphate import in plants: focus on the PHT1 transporters
journal, January 2011
- Nussaume, Laurent
- Frontiers in Plant Science, Vol. 2
A Central Regulatory System Largely Controls Transcriptional Activation and Repression Responses to Phosphate Starvation in Arabidopsis
journal, September 2010
- Bustos, Regla; Castrillo, Gabriel; Linhares, Francisco
- PLoS Genetics, Vol. 6, Issue 9
Complex Regulation of Plant Phosphate Transporters and the Gap between Molecular Mechanisms and Practical Application: What Is Missing?
journal, March 2016
- Gu, Mian; Chen, Aiqun; Sun, Shubin
- Molecular Plant, Vol. 9, Issue 3
Maintenance of phosphate homeostasis and root development are coordinately regulated by MYB1, an R2R3-type MYB transcription factor in rice
journal, May 2017
- Gu, Mian; Zhang, Jun; Li, Huanhuan
- Journal of Experimental Botany, Vol. 68, Issue 13
OsWRKY74 , a WRKY transcription factor, modulates tolerance to phosphate starvation in rice
journal, December 2015
- Dai, Xiaoyan; Wang, Yuanyuan; Zhang, Wen-Hao
- Journal of Experimental Botany, Vol. 67, Issue 3
Phosphate transport in Arabidopsis : Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments
journal, August 2004
- Shin, Heungsop; Shin, Hwa-Soo; Dewbre, Gary R.
- The Plant Journal, Vol. 39, Issue 4
Phosphate Starvation Responses and Gibberellic Acid Biosynthesis are Regulated by the MYB62 Transcription Factor in Arabidopsis
journal, January 2009
- Devaiah, Ballachanda N.; Madhuvanthi, Ramaiah; Karthikeyan, Athikkattuvalasu S.
- Molecular Plant, Vol. 2, Issue 1
A Rice cis -Natural Antisense RNA Acts as a Translational Enhancer for Its Cognate mRNA and Contributes to Phosphate Homeostasis and Plant Fitness
journal, October 2013
- Jabnoune, Mehdi; Secco, David; Lecampion, Cécile
- The Plant Cell, Vol. 25, Issue 10
Phosphorus Dynamics: From Soil to Plant
journal, May 2011
- Shen, Jianbo; Yuan, Lixing; Zhang, Junling
- Plant Physiology, Vol. 156, Issue 3
Physical and Functional Interactions between Pathogen-Induced Arabidopsis WRKY18, WRKY40, and WRKY60 Transcription Factors
journal, April 2006
- Xu, Xinping; Chen, Chunhong; Fan, Baofang
- The Plant Cell, Vol. 18, Issue 5
Plastic transport systems of rice for mineral elements in response to diverse soil environmental changes
journal, December 2019
- Wang, Peitong; Yamaji, Naoki; Inoue, Komaki
- New Phytologist, Vol. 226, Issue 1
Auxin response factor (OsARF12), a novel regulator for phosphate homeostasis in rice ( Oryza sativa )
journal, September 2013
- Wang, SuiKang; Zhang, SaiNa; Sun, ChenDong
- New Phytologist, Vol. 201, Issue 1
Arabidopsis WRKY45 Transcription Factor Activates PHOSPHATE TRANSPORTER1;1 Expression in Response to Phosphate Starvation
journal, February 2014
- Wang, Hui; Xu, Qian; Kong, You-Han
- Plant Physiology, Vol. 164, Issue 4
Regulation of rice responses to submergence by WRKY transcription factors
journal, September 2018
- Viana, V. E.; Marini, N.; Busanello, C.
- Biologia plantarum, Vol. 62, Issue 3
The WRKY Gene Family in Rice (Oryza sativa)
journal, June 2007
- Ross, Christian A.; Liu, Yue; Shen, Qingxi J.
- Journal of Integrative Plant Biology, Vol. 49, Issue 6
WRKY transcription factors: from DNA binding towards biological function
journal, October 2004
- Ülker, Bekir; Somssich, Imre E.
- Current Opinion in Plant Biology, Vol. 7, Issue 5
Increased phosphate transport of A rabidopsis thaliana Pht1;1 by site-directed mutagenesis of tyrosine 312 may be attributed to the disruption of homomeric interactions: Pht1;1 Y312 is key to oligomerization and function
journal, April 2015
- Fontenot, Elena B.; Ditusa, Sandra Feuer; Kato, Naohiro
- Plant, Cell & Environment, Vol. 38, Issue 10
The WRKY6 Transcription Factor Modulates PHOSPHATE1 Expression in Response to Low Pi Stress in Arabidopsis
journal, November 2009
- Chen, Yi-Fang; Li, Li-Qin; Xu, Qian
- The Plant Cell, Vol. 21, Issue 11
PROTEIN PHOSPHATASE95 Regulates Phosphate Homeostasis by Affecting Phosphate Transporter Trafficking in Rice
journal, January 2020
- Yang, Zhili; Yang, Jian; Wang, Yan
- The Plant Cell, Vol. 32, Issue 3
Regulation of miR399f Transcription by AtMYB2 Affects Phosphate Starvation Responses in Arabidopsis
journal, November 2012
- Baek, Dongwon; Kim, Min Chul; Chun, Hyun Jin
- Plant Physiology, Vol. 161, Issue 1
A Mutant of the Arabidopsis Phosphate Transporter PHT1;1 Displays Enhanced Arsenic Accumulation
journal, March 2007
- Catarecha, Pablo; Segura, Ma Dolores; Franco-Zorrilla, José Manuel
- The Plant Cell, Vol. 19, Issue 3
Phosphate starvation induced OsPHR4 mediates Pi-signaling and homeostasis in rice
journal, November 2016
- Ruan, Wenyuan; Guo, Meina; Wu, Ping
- Plant Molecular Biology, Vol. 93, Issue 3
Phosphate transporters from the higher plant Arabidopsis thaliana.
journal, September 1996
- Muchhal, U. S.; Pardo, J. M.; Raghothama, K. G.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 19
OsPHR2 Is Involved in Phosphate-Starvation Signaling and Excessive Phosphate Accumulation in Shoots of Plants
journal, February 2008
- Zhou, Jie; Jiao, FangChang; Wu, Zhongchang
- Plant Physiology, Vol. 146, Issue 4
OsPHT1;3 Mediates Uptake, Translocation, and Remobilization of Phosphate under Extremely Low Phosphate Regimes
journal, December 2018
- Chang, Ming Xing; Gu, Mian; Xia, Yu Wei
- Plant Physiology, Vol. 179, Issue 2
OsPHF1 Regulates the Plasma Membrane Localization of Low- and High-Affinity Inorganic Phosphate Transporters and Determines Inorganic Phosphate Uptake and Translocation in Rice
journal, July 2011
- Chen, Jieyu; Liu, Yu; Ni, Jun
- Plant Physiology, Vol. 157, Issue 1
Loss of the Nrf2 transcription factor causes a marked reduction in constitutive and inducible expression of the glutathione S-transferase Gsta1, Gsta2, Gstm1, Gstm2, Gstm3 and Gstm4 genes in the livers of male and female mice
journal, July 2002
- Chanas, Simon A.; Jiang, Qing; McMAHON, Michael
- Biochemical Journal, Vol. 365, Issue 2
Preferential Delivery of Zinc to Developing Tissues in Rice Is Mediated by P-Type Heavy Metal ATPase OsHMA2
journal, April 2013
- Yamaji, Naoki; Xia, Jixing; Mitani-Ueno, Namiki
- Plant Physiology, Vol. 162, Issue 2
Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis
journal, June 2003
- Hiratsu, Keiichiro; Matsui, Kyoko; Koyama, Tomotsugu
- The Plant Journal, Vol. 34, Issue 5
The Diverse Roles of Rice PHO1 in Phosphate Transport: From Root to Node to Grain
journal, July 2020
- Chiou, Tzyy-Jen
- Plant and Cell Physiology, Vol. 61, Issue 8
Involvement of OsPht1;4 in phosphate acquisition and mobilization facilitates embryo development in rice
journal, May 2015
- Zhang, Fang; Sun, Yafei; Pei, Wenxia
- The Plant Journal, Vol. 82, Issue 4
Phosphate Acquisition
journal, June 1999
- Raghothama, K. G.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1
Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants
journal, July 2004
- Misson, Julie; Thibaud, Marie-Christine; Bechtold, Nicole
- Plant Molecular Biology, Vol. 55, Issue 5
Arabidopsis PHL2 and PHR1 Act Redundantly as the Key Components of the Central Regulatory System Controlling Transcriptional Responses to Phosphate Starvation
journal, November 2015
- Sun, Lichao; Song, Li; Zhang, Ye
- Plant Physiology, Vol. 170, Issue 1