Abstract
Overexpression of OsPHR2 increases phosphate (Pi) uptake and causes overaccumulation of Pi in rice plants, which is toxic to rice plants when they are grown in media with a sufficient Pi supply. The toxicity that results from OsPHR2 overexpression can be significantly relieved by growing the plants in a waterlogged paddy field. A comparison of the Pi uptake and growth status of OsPHR2-overexpression plants (PHR2-Oe plants) grown in paddy fields or in a laboratory setting in aerated or stagnant hydroponic conditions indicated that the oxygen limitation that is present in paddy fields and in stagnant rice culture solutions inhibits the Pi overaccumulation toxicity of PHR2-Oe plants by reducing their Pi uptake. Quantitative RT-PCR demonstrated that the expression of Pi-starvation-induced (PSI) genes was induced by oxygen limitation in both wild-type and PHR2-Oe plants. The induction of PSI genes is the consequence of reducing the Pi concentration in stagnant plants. Thus, when evaluating the efficiency of Pi use in rice germplasm or transgenic materials under hydroponic conditions, the impact of the low oxygen condition that exists in waterlogged paddies should be considered.
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References
Armstrong W, Drew M (2002) Root growth and metabolism under oxygen deficiency. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 729–761
Chiou TJ, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206
Colmer TD, Greenway H (2011) Ion transport in seminal and adventitious roots of cereals during O2 deficiency. J Exp Bot 62:39–57
Colmer TD, Pedersen O (2008) Oxygen dynamics in submerged rice (Oryza sativa). New Phytol 178:326–334
Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034
Garthwaite AJ, Armstrong W, Colmer TD (2008) Assessment of O2 diffusivity across the barrier to radial O2 loss in adventitious roots of Hordeum marinum. New Phytol 179:405–416
Hammond JP, White PJ (2011) Sugar signaling in root responses to low phosphorus availability. Plant Physiol 156:1033–1040
Hattori Y, Nagai K, Ashikari M (2011) Rice growth adapting to deepwater. Curr Opin Plant Biol 14:100–105
Huang S, Colmer TD, Millar AH (2008) Does anoxia tolerance involve altering the energy currency towards PPi? Trends Plant Sci 13:221–227
Huang TK, Han CL, Lin SI, Chen YJ, Tsai YC, Chen YR, Chen JW, Lin WY, Chen PM, Liu TY, Chen YS, Sun CM, Chiou TJ (2013) Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots. Plant Cell 25:4044–4060
Huguenin-Elie O, Kirk GJ, Frossard E (2009) The effects of water regime on phosphorus responses of rainfed lowland rice cultivars. Ann Bot 103:211–220
Insalud N, Bell RW, Colmer TD, Rerkasem B (2006) Morphological and physiological responses of rice (Oryza sativa) to limited phosphorus supply in aerated and stagnant solution culture. Ann Bot 98:995–1004
Kawano N, Ito O, Sakagami J (2009) Morphological and physiological responses of rice seedlings to complete submergence (flash flooding). Ann Bot 103:161–169
Lai F, Thacker J, Li Y, Doerner P (2007) Cell division activity determines the magnitude of phosphate starvation responses in Arabidopsis. Plant J 50:545–556
Lei M, Zhu C, Liu Y, Karthikeyan AS, Bressan RA, Raghothama KG, Liu D (2011) Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. New Phytol 189:1084–1095
Lin WY, Huang TK, Chiou TJ (2013) Nitrogen limitation adaptation, a target of microRNA827, mediates degradation of plasma membrane-localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis. Plant Cell 25:4061–4074
Liu F, Wang Z, Ren H, Shen C, Li Y, Ling HQ, Wu C, Lian X, Wu P (2010) OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice. Plant J 62:508–517
Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049
Pedersen O, Rich SM, Colmer TD (2009) Surviving floods: leaf gas films improve O(2) and CO(2) exchange, root aeration, and growth of completely submerged rice. Plant J 58:147–156
Secco D, Wang C, Arpat BA, Wang Z, Poirier Y, Tyerman SD, Wu P, Shou H, Whelan J (2012) The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytol 193:842–851
Shiono K, Ogawa S, Yamazaki S, Isoda H, Fujimura T, Nakazono M, Colmer TD (2011) Contrasting dynamics of radial O2-loss barrier induction and aerenchyma formation in rice roots of two lengths. Ann Bot 107:89–99
Tian J, Wang C, Zhang Q, He X, Whelan J, Shou H (2012) Overexpression of OsPAP10a, a root-associated acid phosphatase, increased extracellular organic phosphorus utilization in rice. J Integr Plant Biol 54:631–639
Vance CP (2010) Quantitative trait loci, epigenetics, sugars, and MicroRNAs: quaternaries in phosphate acquisition and use. Plant Physiol 154:582–588
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447
Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible W-R, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195:306–320
Vreeburg RA, Benschop JJ, Peeters AJ, Colmer TD, Ammerlaan AH, Staal M, Elzenga TM, Staals RH, Darley CP, McQueen-Mason SJ, Voesenek LA (2005) Ethylene regulates fast apoplastic acidification and expansin A transcription during submergence-induced petiole elongation in Rumex palustris. Plant J 43:597–610
Wang C, Ying S, Huang H, Li K, Wu P, Shou H (2009) Involvement of OsSPX1 in phosphate homeostasis in rice. Plant J 57:895–904
Wang C, Huang W, Ying Y, Li S, Secco D, Tyerman S, Whelan J, Shou H (2012) Functional characterization of the rice SPX-MFS family reveals a key role of OsSPX-MFS1 in controlling phosphate homeostasis in leaves. New Phytol 196:139–148
Wu P, Shou H, Xu G, Lian X (2013) Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr Opin Plant Biol 16:205–212
Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. The International Rice Research Institute, Manila
Yu H, Luo N, Sun L, Liu D (2012) HPS4/SABRE regulates plant responses to phosphate starvation through antagonistic interaction with ethylene signalling. J Exp Bot 63:4527–4538
Zhang Q, Wang C, Tian J, Li K, Shou H (2011) Identification of rice purple acid phosphatases related to phosphate starvation signalling. Plant Biol 13:7–15
Zheng L, Huang F, Narsai R, Wu J, Giraud E, He F, Cheng L, Wang F, Wu P, Whelan J, Shou H (2009) Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol 151:262–274
Zhou J, Jiao F, Wu Z, Li Y, Wang X, He X, Zhong W, Wu P (2008) OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol 146:1673–1686
Acknowledgments
This work was supported by the Key Basic Research Special Foundation of China (2011CB100303), the National Science Foundation of China (31172024 and 31201675), and the Ministry of Science and Technology of China (2013ZX08004-001-03 and 2013ZX08003005-001).
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Li, S., Wang, C., Zhou, L. et al. Oxygen deficit alleviates phosphate overaccumulation toxicity in OsPHR2 overexpression plants. J Plant Res 127, 433–440 (2014). https://doi.org/10.1007/s10265-014-0628-0
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DOI: https://doi.org/10.1007/s10265-014-0628-0