https://doi.org/10.4081/ija.2023.2181
Systemic adaptation of rice plants under low phosphate conditions and interaction with endophytic bacteria
Published: 4 April 2023
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Phosphate (Pi) is essential for plants. Plants have adapted mechanisms to overcome Pi deficiencies. This study examined the interaction of two contrasting rice varieties (G22 and G299) and two endophytic bacterial strains. Four different culture media were established: full Pi (P0), Pi starvation (P*), insoluble Pi with Pi-solubilizing Burkholderia sp. strain 205 (P+205), or Pi-insolubilizing strain 113 (P+113). We investigated the responses of rice to these media. Root length and weight and the number of crown roots were higher in the P* and P+113 medium than the two other media. However, shoot length, and weight were lower. Most amino acid families were higher in the P+113 medium than in the other media. The roots of G299 plants in the P+113 medium showed the highest relative expression of all phosphate-analyzed genes; however, these genes were expressed at low levels in the leaves of both rice varieties. Notably, the jasmonic acid gene OsJAZ5 showed the highest expression in the roots of G299 plants in the P+113 medium. Our results demonstrate the strong effects of the different genetic backgrounds of bacteria and rice plants on the response to low Pi. We also demonstrate the involvement of jasmonic acid in low Pi and soluble-phosphate-bacteria interaction in G299 plants. A positive interaction between Burkholderia sp. strain 205 and rice plants has been noticed in the promotion of plant growth. Further studies under field conditions should be undertaken to develop this potential strain as a biofertilizer.
Adhikari A, Lee KE, Khan MA, Kang SM, Adhikari B, Imran M, Jan R, Kim KM, Lee IJ, 2020. Effect of silicate and phosphate solubilizing rhizobacterium enterobacter ludwigii GAK2 on oryza sativa L. under cadmium stress. J Microbiol. Biotechnol. 30:118-26.
DOI: https://doi.org/10.4014/jmb.1906.06010
Afzal I, Shinwari ZK, Sikandar S, Shahzad S, 2019. Plant beneficial endophytic bacteria: mechanisms, diversity, host range and genetic determinants. Microbiol. Res. 221:36-49.
DOI: https://doi.org/10.1016/j.micres.2019.02.001
Alori ET, Glick BR, Babalola OO, 2017. Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front. Microbiol. 8:971.
DOI: https://doi.org/10.3389/fmicb.2017.00971
Babalola OO, Bernard RG, 2012. The use of microbial inoculants in African agriculture: current practice and future prospects. J. Food Agric. Environ. 10:540-9.
Baqual MF, Das PK, 2006. Influence of Biofertilizers on Macronutrient uptake by the Mulberry Plant and its Impact on Silkworm Bioassay. Caspian J. Env. Sci. 4:98-109.
Bargaz A, Elhaissoufi W, Khourchi S, Benmrid B, .Borden KA, Rchiad Z, 2021. Benefits of phosphate solubilizing bacteria on belowground crop performance for improved crop acquisition of phosphorus. Microbiol. Research. 252:126842.
DOI: https://doi.org/10.1016/j.micres.2021.126842
Barra PJ, Viscardi S, Jorquera MA, Duran PA, Valentine AJ, de la Luz Mora M, 2018. Understanding the strategies to overcome phosphorus–deficiency and aluminum–toxicity by ryegrass endophytic and rhizosphere phosphobacteria. Front. Microbiol. 9:1155.
DOI: https://doi.org/10.3389/fmicb.2018.01155
Batista-Silva W, Heinemann B, Rugen N, Nunes-Nesi A, Araújo WL, Braun HP, Hildebrandt TM, 2019. The role of amino acid metabolism during abiotic stress release. Plant Cell Env. 42:1630-44.
DOI: https://doi.org/10.1111/pce.13518
Bechtaoui N, Rabiu MK, Raklami A, Oufdou K, Hafidi M, Jemo M, 2021. Phosphate-dependent regulation of growth and stresses management in plants. Front. Plant Sci. 12:2357.
DOI: https://doi.org/10.3389/fpls.2021.679916
Chhabra S, Dowling DN, 2017. Endophyte-Promoted Nutrient Acquisition: Phosphorus and Iron. In: Doty S. (eds). Functional Importance of the Plant Microbiome. Springer Cham. pp. 21-4.
DOI: https://doi.org/10.1007/978-3-319-65897-1_3
Charana Walpola B, 2012. Prospectus of phosphate solubilizing microorganisms and phosphorus availability in agricultural soils: a review increase the dissolution rate of eppawala rock phosphate (erp) by using phosphate solubilizing microorganisms. African J. Microbiol. 6:6600-5.
DOI: https://doi.org/10.5897/AJMR12.889
Chea L, Pfeiffer B, Schneider D, Daniel R, Pawelzik E, Naumann M, 2021. Morphological and metabolite responses of potatoes under various phosphorus levels and their amelioration by plant growth-promoting rhizobacteria. Int. J. Mol. Sci. 22:5162.
DOI: https://doi.org/10.3390/ijms22105162
Chen Q, Liu S, 2019. Identification and characterization of the phosphate-solubilizing bacterium pantoea sp. S32 in reclamation soil in Shanxi, China. Front. Microbiol. 10:2171.
DOI: https://doi.org/10.3389/fmicb.2019.02171
Compant S, Kaplan H, Sessitsch A, Nowak J, Ait Barka E, Clément C, 2008. Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol. Ecol. 63:84–93.
DOI: https://doi.org/10.1111/j.1574-6941.2007.00410.x
Crombez H, Motte H, Beeckman T, 2019. Tackling Plant Phosphate Starvation by the Roots. Dev. Cell 48:599-615.
DOI: https://doi.org/10.1016/j.devcel.2019.01.002
Deng Q, Dai L, Chen Y, Wu D, Shen Y, Xie J, Luo X, 2022. Identification of phosphorus stress related proteins in the seedlings of dongxiang wild rice (oryza rufipogon griff.) using label-free quantitative proteomic analysis. Genes.13:108.
DOI: https://doi.org/10.3390/genes13010108
Deng QW, Luo XD, Chen YL, Zhou Y, Zhang FT, Hu BL, Xie JK, 2018. Transcriptome analysis of phosphorus stress responsiveness in the seedlings of dongxiang wild rice (oryza rufipogon griff.). Biol. Res. 51:1-12.
DOI: https://doi.org/10.1186/s40659-018-0155-x
Ezawa T, Smith SE, Smith FA, 2002. P metabolism and transport in AM fungi. Plant Soil 244:221-30.
DOI: https://doi.org/10.1007/978-94-017-1284-2_21
Haefele SM, Nelson A, Hijmans RJ, 2014. Soil quality and constraints in global rice production. Geoderma 235–236:250–9.
DOI: https://doi.org/10.1016/j.geoderma.2014.07.019
Halkier BA, Gershenzon J, 2006. Biology and Biochemistry of Glucosinolates. Annu. Rev. Plant Biol. 57:303-33.
DOI: https://doi.org/10.1146/annurev.arplant.57.032905.105228
Hirsch J, Marin E, Floriani M, Chiarenza S, Richaud P, Nussaume L, Thibaud MC, 2006. Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants. Biochimie. 88:1767-71.
DOI: https://doi.org/10.1016/j.biochi.2006.05.007
Huang CY, Roessner U, Eickmeier I, Genc Y, Callahan DL, Shirley N, Langridge P, Bacic A, 2008. Metabolite profiling reveals distinct changes in carbon and nitrogen metabolism in phosphate-deficient barley plants (Hordeum vulgare L.). Plant Cell Physiol. 49:691-703.
DOI: https://doi.org/10.1093/pcp/pcn044
Jia X, Ye J, Wang H, Li L, Wang F, Zhang Q, Chen J, Zheng X, He H, 2018. Characteristic amino acids in tea leaves as quality indicator for evaluation of Wuyi Rock Tea in different cultured regions. J. Appl. Bot. Food Qual. 91:187-93.
Jiang C, Gao X, Liao L, Harberd NP, Fu X, 2007. Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in arabidopsis. Plant Physiol. 145:1460-70.
DOI: https://doi.org/10.1104/pp.107.103788
Jilani G, Akram A, Ali RM, Hafeez FY, Shamsi IH, Chaudhry AN, Chaudhry AG, 2007. Enhancing crop growth, nutrients availability, economics and beneficial rhizosphere microflora through organic and biofertilizers. Ann. Microbiol. 57:177-84.
DOI: https://doi.org/10.1007/BF03175204
Kariman K, Barker SJ, Finnegan PM, Tibbett M, 2014. Ecto- and arbuscular mycorrhizal symbiosis can induce tolerance to toxic pulses of phosphorus in jarrah (Eucalyptus marginata) seedlings. Mycorrhiza 24:501-9.
DOI: https://doi.org/10.1007/s00572-014-0567-6
King E, Wallner A, Rimbault E, Barrachina C, Klonowska A, Moulin L, Czernic P, 2019. Monitoring of rice transcriptional responses to contrasted colonizing patterns of phytobeneficial burkholderia s.l. reveals a temporal shift in ja systemic response. Front. Plant Sci. 10:1141.
DOI: https://doi.org/10.3389/fpls.2019.01141
Kirkby EA, Johnston AE, 2008. Soil and fertilizer phosphorus in relation to crop nutrition.In: White PJ, Hammond JP (eds). The ecophysiology of plant-phosphorus interactions. Plant ecophysiology, vol 7. Dordrecht: Springer. pp. 177-223.
DOI: https://doi.org/10.1007/978-1-4020-8435-5_9
Kobayashi T, Itai RN, Senoura T, Oikawa T, Ishimaru Y, Ueda M, Nakanishi H, Nishizawa NK, 2016. Jasmonate signaling is activated in the very early stages of iron deficiency responses in rice roots. Plant Mol. Biol. 91:533-47.
DOI: https://doi.org/10.1007/s11103-016-0486-3
Kumar S, Pallavi, Chugh C, Seem K, Kumar S, Vinod KK, Mohapatra T, 2021. Characterization of contrasting rice (Oryza sativa L.) genotypes reveals the Pi-efficient schema for phosphate starvation tolerance. BMC. Plant Biol. 21:282.
DOI: https://doi.org/10.1186/s12870-021-03015-4
Li L, Liu C, Lian X, 2010. Gene expression profiles in rice roots under low phosphorus stress. Plant Mol. Biol. 72:423-32.
DOI: https://doi.org/10.1007/s11103-009-9580-0
Liang C, Wang J, Zhao J, Tian J, Liao H, 2014. Control of phosphate homeostasis through gene regulation in crops. Curr. Opin. Plant Biol. 21:59-66.
DOI: https://doi.org/10.1016/j.pbi.2014.06.009
Lindsay WL, 1979. Chemical equilibria in soils. Clays Clay Miner. 28:319.
DOI: https://doi.org/10.1346/CCMN.1980.0280411
Liu G, Ji Y, Bhuiyan NH, Pilot G, Selvaraj G, Zou J, Wei Y, 2010. Amino acid homeostasis modulates salicylic acid–associated redox status and defense responses in arabidopsis. Plant Cell. 22:3845.
DOI: https://doi.org/10.1105/tpc.110.079392
Livak KJ, Schmittgen TD, 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402-8.
DOI: https://doi.org/10.1006/meth.2001.1262
López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L, 2003. The role of nutrient availability in regulating root architecture. Curr. Opin. Plant Biol. 6:280-7.
DOI: https://doi.org/10.1016/S1369-5266(03)00035-9
Luo X, Li Z, Xiao S, Ye Z, Nie X, Zhang X, Kong J, Zhu L, 2021. Phosphate deficiency enhances cotton resistance to Verticillium dahliae through activating jasmonic acid biosynthesis and phenylpropanoid pathway. Plant Sci. 302:110724.
DOI: https://doi.org/10.1016/j.plantsci.2020.110724
Lynch JP, Brown KM, 2001. Topsoil foraging – an architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225-37.
DOI: https://doi.org/10.1023/A:1013324727040
Mai NTP, Mai CD, Nguyen H Van, Le KQ, Duong LV, Tran TA, To HTM, 2021. Discovery of new genetic determinants of morphological plasticity in rice roots and shoots under phosphate starvation using GWAS. J. Plant Physiol. 257:153340.
DOI: https://doi.org/10.1016/j.jplph.2020.153340
Mattos KA, Pádua VLM, Romeiro A, Hallack LF, Neves BC, Ulisses TMU, Barros CF, Todeschini AR, Previato JO, Mendonça-Previato L, 2008. Endophytic colonization of rice (Oryza sativa L.) by the diazotrophic bacterium Burkholderia kururiensis and its ability to enhance plant growth. An. Acad. Bras. Cienc. 80:477-93.
DOI: https://doi.org/10.1590/S0001-37652008000300009
Mei C, Chretien RL, Amaradasa BS, He Y, Turner A, Lowman S, 2021. Characterization of phosphate solubilizing bacterial endophytes and plant growth promotion in vitro and in greenhouse. Microorganisms 9:1935.
DOI: https://doi.org/10.3390/microorganisms9091935
Oliva M, Guy A, Galili G, Dor E, Schweitzer R, Amir R, Hacham Y, 2021. Enhanced production of aromatic amino acids in tobacco plants leads to increased phenylpropanoid metabolites and tolerance to stresses. Front. Plant Sci. 11:2110.
DOI: https://doi.org/10.3389/fpls.2020.604349
Paz-Ares J, Puga MI, Rojas-Triana M, Martinez-Hevia I, Diaz S, Poza-Carrión C, Miñambres M, Leyva A, 2022. Plant adaptation to low phosphorus availability: core signaling, crosstalks, and applied implications. Mol. Plant 15:104-24.
DOI: https://doi.org/10.1016/j.molp.2021.12.005
Raj DP, 2014. Molecular characterization of Phosphate Solubilizing Bacteria (PSB) and Plant Growth Promoting Rhizobacteria (PGPR) from pristine soils. Int. J. Innov. Sci. Eng. Technol. 1:317-24.
Sabbioni G, Funck D, Forlani G, 2021. Enzymology and regulation of δ1-Pyrroline-5-carboxylate synthetase 2 from rice. Front. Plant Sci. 12:1894.
DOI: https://doi.org/10.3389/fpls.2021.672702
Secco D, Baumann A, Poirier Y, 2010. 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. Plant Physiol. 152:1693-704.
DOI: https://doi.org/10.1104/pp.109.149872
Singh AP, Pandey BK, Deveshwar P, Narnoliya L, Parida SK, Giri J, 2015. JAZ repressors: potential involvement in nutrients deficiency response in rice and chickpea. Front. Plant Sci. 6:975.
DOI: https://doi.org/10.3389/fpls.2015.00975
Shin H, Shin HS, Dewbre GR, Harrison MJ, 2004. Phosphate transport in arabidopsis: Pht1;1 and Pht1; 4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J. 39:629-42.
DOI: https://doi.org/10.1111/j.1365-313X.2004.02161.x
Stephen J, Shabanamol S, Rishad KS, Jisha MS, 2015. Growth enhancement of rice (Oryza sativa) by phosphate solubilizing Gluconacetobacter sp. (MTCC 8368) and Burkholderia sp. (MTCC 8369) under greenhouse conditions. 3 Biotech. 5:831-7.
DOI: https://doi.org/10.1007/s13205-015-0286-5
Székely G, Ábrahám E, Cséplo Á, Rigó G, Zsigmond L, Csiszár J, Ayaydin F, Strizhov N, Jásik J, Schmelzer E, Koncz C, Szabados L, 2008. Duplicated P5CS genes of arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J. 53:11-28.
DOI: https://doi.org/10.1111/j.1365-313X.2007.03318.x
Tajini F, Trabelsi M, Drevon JJ, 2012. Combined inoculation with glomus intraradices and Rhizobium tropici CIAT899 increases phosphorus use efficiency for symbiotic nitrogen fixation in common bean (Phaseolus vulgaris L.). Saudi J. Biol. Sci. 19:157-63.
DOI: https://doi.org/10.1016/j.sjbs.2011.11.003
Tawaraya K, 2022. Response of mycorrhizal symbiosis to phosphorus and its application for sustainable crop production and remediation of environment. Soil Sci. Plant Nutr. 68:1-5.
DOI: https://doi.org/10.1080/00380768.2022.2032335
To TMH, Nguyen TH, Dang TMN, Nguyen HN, Bui XT, Lavarenne J, Phung TPN, Gantet, P, Lebrun M, Bellafiore S, Champion A, 2019. Unraveling the genetic elements involved in shoot and root growth regulation by jasmonate in rice using a genome-wide association study. Rice (N Y). 12:69.
DOI: https://doi.org/10.1186/s12284-019-0327-5
To HTM, Le KQ, Van Nguyen H, Duong LV, Kieu HT, Chu QAT, Tran TP, Mai NTP, 2020. A genome-wide association study reveals the quantitative trait locus and candidate genes that regulate phosphate efficiency in a Vietnamese rice collection. Physiol. Mol. Biol. Plants 26:2267-81.
DOI: https://doi.org/10.1007/s12298-020-00902-2
Trovato M, Funck D, Forlani G, Okumoto S, Amir R, 2021. Editorial: amino acids in plants: regulation and functions in development and stress defense. Front. Plant Sci. 12:2287.
DOI: https://doi.org/10.3389/fpls.2021.772810
Varga T, Hixson KK, Ahkami AH, Sher AW, Barnes ME, Chu RK, Battu AK, Nicora CD, Winkler TE, Reno LR, Fakra SC, Antipova O, Parkinson DY, Hall JR, Doty SL, 2020. Endophyte-promoted phosphorus solubilization in populus. Front. Plant Sci. 11:1585.
DOI: https://doi.org/10.3389/fpls.2020.567918
Wang X, Wang Y, Piñeros MA, Wang Z, Wang W, Li C, Wu Z, Kochian L V., Wu P, 2014. Phosphate transporters OsPHT1; 9 and OsPHT1; 10 are involved in phosphate uptake in rice. Plant. Cell Environ. 37:1159-70.
DOI: https://doi.org/10.1111/pce.12224
Wang Z, Xu G, Ma P, Lin Y, Yang X, Cao C, 2017. Isolation and characterization of a phosphorus-solubilizing bacterium from rhizosphere soils and its colonization of Chinese cabbage (Brassica campestris ssp. chinensis). Front. Microbiol. 8:1270.
DOI: https://doi.org/10.3389/fmicb.2017.01270
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.
DOI: https://doi.org/10.1111/j.1365-313X.2008.03734.x
Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, Deng XW, 2003. Phosphate starvation triggers distinct alterations of genome expression in arabidopsis roots and leaves. Plant Physiol. 132:1260-71.
DOI: https://doi.org/10.1104/pp.103.021022
Yoshida S, Forno DA, Cock J, 1971. Laboratory Manual for Physiological Studies of Rice. Available from: http://books.irri.org/9711040352_content.pdf.
Zhang J, Liu YX, Zhang N, Hu B, Jin T, Xu H, Qin Y, Yan P, Zhang X, Guo X, Hui J, Cao S, Wang X, Wang C, Wang H, Qu B, Fan G, Yuan L, Garrido-Oter R, Chu C, Bai Y, 2019a. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat Biotechnol. 37:676-84.
DOI: https://doi.org/10.1038/s41587-019-0104-4
Zhang J, Jiang F, Shen Y, Zhan Q, Bai B, Chen W, Chi Y, 2019b. Transcriptome analysis reveals candidate genes related to phosphorus starvation tolerance in sorghum. BMC Plant Biol. 19:1-18.
DOI: https://doi.org/10.1186/s12870-019-1914-8
Zhang Q, Wang C, Tian J, Li K, Shou H, 2011. Identification of rice purple acid phosphatases related to phosphate starvation signalling. Plant Biol. (Stuttg). 13:7-15.
DOI: https://doi.org/10.1111/j.1438-8677.2010.00346.x
Zhou J, Jiao FC, 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. 146:1673-86.
DOI: https://doi.org/10.1104/pp.107.111443
How to Cite
Nguyen, V. P., Anh Le, T. V., Mai To, H. T., Oanh Nguyen, T. K., & Mai, N. T. P. (2023). Systemic adaptation of rice plants under low phosphate conditions and interaction with endophytic bacteria. Italian Journal of Agronomy, 18(1). https://doi.org/10.4081/ija.2023.2181
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