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A 1.84-Mb region on rice chromosome 2 carrying SPL4, SPL5 and MLO8 genes is associated with higher yield under phosphorus-deficient acidic soil

  • Plant Genetics • Original Paper
  • Published:
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Abstract

Phosphorus (P) deficiency is one of the major limiting factors for rice productivity with only one locus (PSTOL1) available for field based application. A biparental mapping population (F6) derived from two P deficiency tolerant genotypes (Sahbhagi Dhan (SD) (PSTOL1+) and Chakhao Poreiton (CP) (PSTOL1−)), in which, transcriptome data generated from our lab had previously shown existence of diverse mechanisms was used to identify novel regions for better yield under lowland acidic soils. Phenotyping at F4, F5 and F6 generations revealed significant correlation between traits like tiller number at 30 days (TN 30), tiller number at 60 days (TN 60), filled grains (FG), percent spikelet fertility (SF%), panicle number (PN) and grain yield per panicle (GYPP) and also association with better yield/performance under low P acidic soil conditions. Through selected genotyping on a set of forty superior and inferior lines using SSR, candidate gene–based and SNP polymorphic markers, 5 genomic regions associated with various yield-related traits were identified. Marker trait association studies revealed 13 markers significantly associated with yield attributing traits and PUE under lowland acidic field conditions. Chi-square and regression analyses of markers run on the entire population identified seven and six markers for SF% and GYPP, respectively, and two for biological yield with positive allele derived from SD which constitute a novel 1.847-Mb region on chromosome 2 flanked by two markers RM12550 and PR9-2. Expression analysis of 7 candidate genes lying within this region across SD, CP and two low P susceptible rice genotypes has revealed that expression of four genes including SPL4, SPL5, ACA9 and MLO8 is significantly upregulated only in SD under low P conditions. In CP, there is low expression of MLO8 under low P conditions, whereas SPL4, SPL5 and Os02g08120 are downregulated. In the case of the two susceptible genotypes, there is no expression of Os02g08120 either in optimum or limiting conditions. Sequence data across a panel of 3024 rice genotypes also suggests that there is polymorphism for these differentially expressed genes. The genes and underlying markers identified on chromosome 2 will be key to imparting tolerance to low P in diverse genetic backgrounds and for marker-assisted selection for higher yield under lowland acidic conditions.

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References

  • Ali J, Jewel ZA, Mahender A, Anandan A, Hernandez J, Li Z (2018) Molecular genetics and breeding for nutrient use efficiency in rice. Int J Mol Sci 19:E1762

    Article  PubMed  Google Scholar 

  • Bhutia KL, Nongbri EL, Gympad E, Rai M, Tyagi W (2020) In silico characterization, and expression analysis of rice golden 2-like (OsGLK) members in response to low phosphorous. Mol Biol Rep 47:2529

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Liu Y, Ni J, Wang Y, Bai Y, Shi J, Gan J, Wu Z, Wu P (2011) OsPHF1 regulates the plasma membrane localization of low- and high-affinity inorganic phosphate transporters and determines inorganic phosphate uptake and translocation in rice. Plant Physiol 157:269–278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chin JH, Lu X, Haefele SM, Gamuyao R, Ismail AM, Wissuwa M, Heuer S (2010) Development and application of gene-based markers for the major rice QTL phosphorus uptake 1. Theor Appl Genet 120:1073–1086

    Article  CAS  PubMed  Google Scholar 

  • Das S, Tyagi W, Rai M, Yumnam JS (2017) Understanding Fe2+ toxicity and P deficiency tolerance in rice for enhancing productivity under acidic soils. Biotechol Genetic Eng 33:97–117

    Article  Google Scholar 

  • Delgado M, Zúñiga-Feest A, Almonacid L, Lambers H, Borie F (2015) Cluster roots of Embothrium coccineum (Proteaceae) affect enzyme activities and phosphorus lability in rhizosphere soil. Plant Soil 395:189–200

    Article  CAS  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1:19–21

    Article  CAS  Google Scholar 

  • Deng Q-W, Luo X-D, Chen Y-L, Zhou Y, Zhang F-T, Biao-Lin Hu B-L, Xie J-K (2018) Transcriptome analysis of phosphorus stress responsiveness in the seedlings of Dongxiang wild rice (Oryza rufipogon Griff.). Biol Res 51:7

    Article  PubMed  PubMed Central  Google Scholar 

  • Domingo C, Lalanne E, Catalá MM, Pla E, Reig-Valiente JL, Talón M (2016) Physiological basis and transcriptional profiling of three salt-tolerant mutant lines of rice. Front Plant Sci 7:1462

    Article  PubMed  PubMed Central  Google Scholar 

  • Dutta SS, Tyagi W, Pale G, Pohlong J, Aochen C, Pandey A, Pattanayak A, Rai M (2018) Marker–trait association for low-light intensity tolerance in rice genotypes from Eastern India. Mol Genet Genomics 293:1493–1506

    Article  CAS  PubMed  Google Scholar 

  • Florez-Sarasa I, Lambers H, Wang X, Finnegan PM, Ribas-Carbo M (2014) The alternative respiratory pathway mediates carboxylate synthesis in white lupin cluster roots under phosphorus deprivation. Plant Cell Environ 37:922–928

    Article  CAS  PubMed  Google Scholar 

  • Gamuyao R, Hyoun CJ, Pariasca TJ, Pesaresi P, Catausan S, Dalid-Gasper C, Slamet-Loedin I, Tecson-Mendoza EM, Wissuwa M, Heuer S (2012) The protein kinase PSTOL1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488:535–539

    Article  CAS  PubMed  Google Scholar 

  • Gong YM, Guo ZH, He LY, Li JS (2011) Identification of maize genotypes with high tolerance or sensitivity to phosphorus deficiency. J Plant Nutr 34:1290–1302

    Article  CAS  Google Scholar 

  • Guo M, Ruan W, Li C, Huang F, Zeng M, Liu Y, Yu Y, Ding X, Wu Z, Mao C, Yi K, Wu P, Mo X (2015) Integrative comparison of the role of the PHOSPHATE RESPONSE1 subfamily in phosphate signaling and homeostasis in rice. Plant Physiol 168:1762–1776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He G, Luo X, Tian F, Li K, Zhu Z, Su W, Qian X, Fu Y, Wang X, Sun C, Yang J (2006) Haplotype variation in structure and expression of a gene cluster associated with a quantitative trait locus for improved yield in rice. Genome Res 16:618–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He Q, Wang F, Wang Y, Lu H, Yang Z, Lv Q, Mao C (2019) Molecular control and genetic improvement of phosphorus use efficiency in rice. Mol Breeding 39:162

    Article  CAS  Google Scholar 

  • Hedley MJ, Kirk GJD, Santos MB (1994) Phosphorus efficiency and the forms of soil phosphorus utilized by upland rice cultivars. Plant Soil 158:53–62

    Article  CAS  Google Scholar 

  • Heuer S, Gaxiola R, Schilling R, Herrera-Estrella L, Lopez-Arredondo D, Wissuwa M, Delhaize E, Rouached H (2017) Improving phosphorus use efficiency: a complex trait with emerging opportunities. Plant J 90:868–885

    Article  CAS  PubMed  Google Scholar 

  • Huang XH, Wei XH, Sang T, Zhao Q, Feng Q (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967

    Article  CAS  PubMed  Google Scholar 

  • Huda KKM, Yadav S, Banu MSA, Trivedi DK, Tuteja N (2013) Genome-wide analysis of plant-type II Ca2+ ATPases gene family from rice and Arabidopsis: potential role in abiotic stresses. Plant Physiol Biochem 65:32–47

    Article  Google Scholar 

  • Ismail AM, Heuer S, Thomson MJ, Wissuwa M (2007) Genetic and genomic approaches to develop rice germplasm for problem soils. Plant Mol Biol 65:547–570

    Article  CAS  PubMed  Google Scholar 

  • Jewel ZA, Jauhar AJ, Pang Y, Li Z (2019) Identification of quantitative trait loci associated with nutrient use efficiency traits, using SNP markers in an early backcross population of rice (Oryza sativa L.). Int J Mol Sci 20:900

    Article  CAS  PubMed Central  Google Scholar 

  • Jia HF, Ren HY, Gu MY, Zhao JN, Sun SB, Zhang X, Chen J, Wu P, Xu G (2011) The phosphate transporter gene OsPht1; 8 is involved in phosphate homeostasis in rice. Plant Physiol 156:1164–1175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar A, Dixit S, Ram T, Yadav RB, Mishra KK, Mandal NP (2014) Breeding high-yielding drought-tolerant rice: genetic variations and conventional and molecular approaches. J Exp Bot 65:6265–6278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Zhang J, Zhang X, Fan H, Gu M, Qu H (2015) Phosphate transporter OsPht1;8 in rice plays an important role in phosphorus redistribution from source to sink organs and allocation between embryo and endosperm of seeds. Plant Sci 230:23–32

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Wang Z, Ren H, Chenjia S, Li Y, Ling H-Q, 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

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Xu Y, Jiang H, Jiang C, Du Y, Gong C, Wang W, Zhu S, Han G, Cheng B (2016) Systematic identification, evolution and expression analysis of the Zea mays PHT1 gene family reveals several new members involved in root colonization by arbuscular mycorrhizal fungi. Int J Mol Sci 17:930

    Article  PubMed Central  Google Scholar 

  • Lopez-Arredondo DL, Leyva-Gonzalez MA, Gonzalez-Morales SI, Lopez-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123

    Article  CAS  PubMed  Google Scholar 

  • Luo XD, Liu J, Dai LF, Zhang FT, Wan Y, Xie JK (2017) Linkage map construction and QTL identification of P-deficiency tolerance in Oryza rufipogon Griff. at early seedling stage. Euphytica 213:96

    Article  Google Scholar 

  • Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahender A, Swamy BPM, Anandan A, Ali J (2019) Tolerance of iron-deficient and -toxic soil conditions in rice. Plants 8:31

    Article  CAS  PubMed Central  Google Scholar 

  • Mansueto L, Fuentes RR, Borja FN, Detras J, Abriol-Santos JM, Chebotarov D, Sanciangco M, Palis K, Copetti D, Poliakov A, Dubchak I, Solovyev V, Wing RA, Hamilton RS, Mauleon R, McNally KL, Alexandrov N (2017) Rice SNP-Seek Database update: new SNPs, indels, and queries. Nucleic Acids Res 45(D1):D1075–D1081

    Article  CAS  Google Scholar 

  • Marschner P (2012) Mineral nutrition of higher plants, third edn. Academic Press Inc., San Diego

  • Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot 112:391–408

    Article  CAS  PubMed  Google Scholar 

  • Rao R, Neeraja CN, Srikanth B, Subrahmanyam D, Swamy KN, Rajesh K, Vijayalakshmi P, Kiran TV, Sailaja N, Revathi P, Rao PR, Rao LVS, Surekha K, Babhu VR, Voleti SR (2018) Identification of rice landraces with promising yield and the associated genomic regions under low nitrogen. Sci Rep 8:9200

    Article  PubMed  PubMed Central  Google Scholar 

  • Reddy VS, Ali GS, Reddy AS (2002) Genes encoding calmodulin-binding proteins in the Arabidopsis genome. J Biol Chem 277:9840–9852

    Article  CAS  PubMed  Google Scholar 

  • Rose TJ, Wissuwa M (2016) Rethinking internal phosphorus utilization efficiency: a new approach is needed to improve PUE in grain crops. Adv Agron 116:185–217

    Article  Google Scholar 

  • Schiøtt M, Romanowsky SM, Baekgaard L, Jakobsen MK, Palmgren MG, Harper JF (2004) A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci U S A 101:9502–9507

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh H, Singh H, Deshmukh RK, Singh A, Singh AK, Gaikwad K, Sharma TR, Mohapatra T, Singh NK (2010) Highly variable SSR markers suitable for rice genotyping using agarose gels. Mol Breed 25:359–364

    Article  CAS  Google Scholar 

  • Singh D, Singh NP, Chauhan SK, Singh P (2011) Developing aluminium tolerant crop plants using biotechnological tools. Curr Sci 100:1807–1814

    CAS  Google Scholar 

  • Swamy BPM, Ahmed HU, Henry A, Mauleon R, Dixit S, Vikram P, Tilatto R, Satish B, Verulkar SB, Perraju P, Mandal NP, Variar M, Robin S, Chandrababu R, Singh ON, Dwivedi JL, Das SP, Mishra KK, Yadaw RB, Aditya TL, Karmakar B, Satoh K, Moumeni A, Kikuchi S, Leung H, Kumar A (2013) Genetic, physiological, and gene expression analyses reveal that multiple QTL enhance yield of rice mega-variety IR64 under drought. PLoS One 8:e62795

    Article  PubMed  Google Scholar 

  • Tiwari KK, Singh A, Pattnaik S, Sandhu M, Kaur S, Jain S, Tiwari S, Mehrotra S, Anumalla M, Samal R, Bhardwaj J, Dubey N, Sahu V, Kharshing GA, Zeliang PK, Sreenivasan K, Kumar P, Parida SK, Mithra SVA, Rai V, Tyagi W, Agrawal PK, Rao AR, Pattanayak A, Chandel G, Singh AK, Bisht IS, Bhat KV, Rao GJN, Khurana JP, Singh NK, Mohapatra T (2015) Identification of a diverse mini-core panel of Indian rice germplasm based on genotyping using microsatellite markers. Plant Breed 134:164–171

    Article  CAS  Google Scholar 

  • Tyagi W, Rai M (2017) Root transcriptome of two acidic soil adapted Indica rice genotypes suggest diverse and complex mechanism of low phosphorus tolerance. Protoplasma 254:725–736

    Article  CAS  PubMed  Google Scholar 

  • Tyburski J, Dunajska-Ordak K, Skorupa M, Tretyn A (2012) Role of ascorbate in the regulation of the Arabidopsis thaliana root growth by phosphate availability. J Bot 2012:1–11

    Article  Google Scholar 

  • Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15

    Article  Google Scholar 

  • USDA (2018) https://www.fas.usda.gov/data/world-agricultural-production. Accessed 9 March 2019

  • Walder F, Brulé D, Koegel S, Wiemken A, Boller T, Courty P-E (2015) Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. New Phytol 205:1632–1645

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Itaya A, Zhong X, Wu Y, Zhang J, van der Knaap E, Olmstead R, Qi Y, Ding B (2011) Function and evolution of a microRNA that regulates a Ca2+-ATPase and triggers the formation of phased small interfering RNAs in tomato reproductive growth. Plant Cell 23:3185–3203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Zhang S, Sun C, Xu Y, Chen Y, Yu C, Qian Q, Jiang DA, Qi Y (2014a) Auxin response factor (OsARF12), a novel regulator for phosphate homeostasis in rice (Oryza sativa). New Phytol 201:91–103

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Ruan W, Shi J, Zhang L, Xian D, Yang C, Li C, Wu Z, Liu Y, Yu Y, Shou H (2014b) Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc Natl Acad Sci U S A 111:14953–14958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe T, Osaki M, Yano H, Rao IM (2006) Internal mechanisms of plant adaptation to aluminium toxicity and phosphorus starvation in tree tropical forages. J Plant Nutr 29:1243–1255

    Article  CAS  Google Scholar 

  • Wege S, Khan GA, Jung JY, Vogiatzaki E, Pradervand S, Aller I, Meyer AJ, Poirier Y (2016) The EXS domain of PHO1 participates in the response of shoots to phosphate deficiency via a root-to-shoot signal. Plant Physiol 170:385–400

    Article  CAS  PubMed  Google Scholar 

  • White PJ, George TS, Dupuy LX, Karley AJ, Valentine TA, Weisel L, Wishart J (2013) Root traits for infertile soils. Front Plant Sci 4:19

    Article  Google Scholar 

  • Wissuwa M, Ae N (1999) Molecular markers associated with phosphorus uptake and internal phosphorus-use efficiency in rice. In: Gissel-Nielsen G, Jensen A (eds) Plant nutrition—molecular biology and genetics. Kluwer Academic Publishers, The Netherlands, pp 433–439

    Chapter  Google Scholar 

  • Wissuwa M, Yano M, Ae N (1998) Mapping of QTLs for phosphorus deficiency tolerance in rice (Oryza sativa L.). Theor Appl Genet 97:777–783

    Article  CAS  Google Scholar 

  • Wissuwa M, Wegner J, Ae N, Yano M (2002) Substitution mapping of Pup1: a major QTL increasing phosphorus uptake of rice from a phosphorus deficient soil. Theor Appl Genet 105:890–897

    Article  CAS  PubMed  Google Scholar 

  • Wissuwa M, Kretzschmar T, Rose TJ (2016) From promise to application: root traits for enhanced nutrient capture in rice breeding. J Exp Bot 67:3605–3615

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi T, Aharon GS, Sottosanto JB, Blumwald E (2005) Vacuolar Na+/H+ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+-and pH-dependent manner. Proc Natl Acad Sci U S A 102:16107–16112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yumnam JS, Rai M, Tyagi W (2017a) Allele mining across two low-P tolerant genes PSTOL1 and PupK20-2 reveals novel haplotypes in rice genotypes adapted to acidic soils. Plant Genet Resour-C 15:221–229

    Article  CAS  Google Scholar 

  • Yumnam JS, Rai M, Tyagi W (2017b) In silico characterisation of novel rice transcripts differentially expressed in phosphorus deficient conditions suggests a role of these transcripts in multiple abiotic stresses. Acta Biol Hung 68:398–411

    Article  CAS  PubMed  Google Scholar 

  • Yun SJ, Kaeppler SM (2001) Induction of maize acid phosphatase activities under phosphorus starvation. Plant Soil 237:109–115

    Article  CAS  Google Scholar 

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Acknowledgements

Dr. Ng Eng Hwa is acknowledged for facilitating SNP genotyping under CGIAR, HTPG project.

Funding

WT was supported by the grants from Indian Council of Agricultural Research (NAIP; component IV; C30033/415101-036) and Department of Biotechnology, Government of India (BT/566/NE/U-excel/2016/72). KLB was supported by NFST (#201516-NFST-2015-17-ST-3514) from Ministry of Tribal Affairs, University Grant Commission, Government of India.

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  1. Karma Landup Bhutia

    Present address: CBS&H, Dr. Rajendra Prasad Central Agricultural University, Pusa, Bihar, India

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  1. School of Crop Improvement, College of Post Graduate Studies in Agricultural Sciences, Central Agricultural University (Imphal), Umiam, Meghalaya, India

    Karma Landup Bhutia, Ernieca Lyngdoh Nongbri, Takhenchangbam Oshin Sharma, Mayank Rai & Wricha Tyagi

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Contributions

MR and WT conceived the research plan and designed the experiments. KLB performed the phenotyping; KLB, ELN and TOS performed the genotyping. TOS and ELN generated the hydroponics and qRT-PCR data, respectively. KLB wrote the draft. KLB, ELN and TOS analyzed the data generated. WT and MR reviewed and edited the paper, providing helpful comments and discussions. All authors read and approved the final manuscript.

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Correspondence to Wricha Tyagi.

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Bhutia, K.L., Nongbri, E.L., Sharma, T.O. et al. A 1.84-Mb region on rice chromosome 2 carrying SPL4, SPL5 and MLO8 genes is associated with higher yield under phosphorus-deficient acidic soil. J Appl Genetics 62, 207–222 (2021). https://doi.org/10.1007/s13353-020-00601-4

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