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Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency

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Abstract

Strigolactones (SLs) act as plant hormones that inhibit shoot branching and stimulate secondary growth of the stem, primary root growth, and root hair elongation. In the moss Physcomitrella patens, SLs regulate branching of chloronemata and colony extension. In addition, SL-deficient and SL-insensitive mutants show delayed leaf senescence. To explore the effects of SLs on leaf senescence in rice (Oryza sativa L.), we treated leaf segments of rice dwarf mutants with a synthetic SL analogue, GR24, and evaluated their chlorophyll contents, ion leakage, and expression levels of senescence-associated genes. Exogenously applied GR24 restored normal leaf senescence in SL-deficient mutants, but not in SL-insensitive mutants. Most plants highly produce endogenous SLs in response to phosphate deficiency. Thus, we evaluated effects of GR24 under phosphate deficiency. Chlorophyll levels did not differ of in the wild-type between the sufficient and deficient phosphate conditions, but increased in the SL-deficient mutants under phosphate deficiency, leading in the strong promotion of leaf senescence by GR24 treatment. These results indicate that the mutants exhibited increased responsiveness to GR24 under phosphate deficiency. In addition, GR24 accelerated leaf senescence in the intact SL-deficient mutants under phosphate deficiency as well as dark-induced leaf senescence. The effects of GR24 were stronger in d10 compared to d17. Based on these results, we suggest that SLs regulate leaf senescence in response to phosphate deficiency.

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Abbreviations

CCD:

Carotenoid cleavage dioxygenase

Chl:

Chlorophyll

SL:

Strigolactone

SAG:

Senescence-associated gene

References

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  CAS  PubMed  Google Scholar 

  • Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from beta-carotene to carlactone, a strigolactone-like plant hormone. Science 335:1348–1351

    Article  CAS  PubMed  Google Scholar 

  • Arite T, Iwata H, Ohshima K, Maekawa M, Nakajima M, Kojima M, Sakakibara H, Kyozuka J (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 51:1019–1029

    Article  CAS  PubMed  Google Scholar 

  • Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50:1416–1424

    Article  CAS  PubMed  Google Scholar 

  • Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8:443–449

    Article  CAS  PubMed  Google Scholar 

  • Bucher M, Rausch C, Daram P (2001) Molecular and biochemical mechanisms of phosphorus uptake into plants. J Plant Nutr Soil Sci 164:209–217

    Article  CAS  Google Scholar 

  • Cai H, Chu Q, Yuan L, Liu J, Chen X, Chen F, Mi G, Zhang F (2012) Identification of quantitative trait loci for leaf area and chlorophyll content in maize (Zea mays) under low nitrogen and low phosphorus supply. Mol Breed 30:251–266

    Article  CAS  Google Scholar 

  • Cook CE, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154:1189–1190

    Article  CAS  PubMed  Google Scholar 

  • de Groot CC, van den Boogaard R, Marcelis LFM, Harbinson J, Lambers H (2003) Contrasting effects of N and P deprivation on the regulation of photosynthesis in tomato plants in relation to feedback limitation. J Exp Bot 54:1957–1967

    Article  PubMed  Google Scholar 

  • Foo E, Yoneyama K, Hugill C, Quittenden L, Reid J (2013) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol Plant 6:76–87

    Article  CAS  PubMed  Google Scholar 

  • Fujiki Y, Sato T, Ito M, Watanabe A (2000) Isolation and characterization of cDNA clones for the E1ß and E2 subunits of the branched-chain α-ketoacid dehydrogenase complex in Arabidopsis. J Biol Chem 275:6007–6013

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194

    Article  CAS  PubMed  Google Scholar 

  • Hamiaux C, Drummond RS, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, Snowden KC (2012) DAD2 is an alpha/beta hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22:2032–2036

    Article  CAS  PubMed  Google Scholar 

  • Hu ZY, Yan HF, Yang JH, Yamaguchi S, Maekawa M, Takamure I, Tsutsumi N, Kyozuka J, Nakazono M (2010) Strigolactones negatively regulate mesocotyl elongation in rice during germination and growth in darkness. Plant Cell Physiol 51:1136–1142

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, Kyozuka J (2005) Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol 46:79–86

    Article  CAS  PubMed  Google Scholar 

  • Jibran R, Hunter DA, Dijkwel PP (2013) Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol Biol 82:547–561

    Article  CAS  PubMed  Google Scholar 

  • Kamachi K, Yamaya T, Mae T, Ojima K (1991) A role for glutamine-synthetase in the remobilization of leaf nitrogen during natural senescence in rice leaves. Plant Physiol 96:411–417

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol 155:974–987

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee RH, Wang CH, Huang LT, Chen SC (2001) Leaf senescence in rice plants: cloning and characterization of senescence up-regulated genes. J Exp Bot 52:1117–1121

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Lim PO, Nam HG (2005) The molecular and genetic control of leaf senescence and longevity in Arabidopsis. Curr Top Dev Biol 67:49–83

    Article  CAS  PubMed  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  CAS  PubMed  Google Scholar 

  • Lin H, Wang RX, Qian Q, Yan MX, Meng XB, Fu ZM, Yan CY, Jiang B, Su Z, Li JY, Wang YH (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21:1512–1525

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lopez-Raez JA, Charnikhova T, Gomez-Roldan V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Becard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Wu YR, Han B (2005) Anaerobic induction of isocitrate lyase and malate synthase in submerged rice seedlings indicates the important metabolic role of the glyoxylate cycle. Acta Biochim Biophys Sin 37:406–414

    Article  CAS  PubMed  Google Scholar 

  • Luquet D, Zhang BG, Dingkuhn M, Dexet A, Clement-Vidal A (2005) Phenotypic plasticity of rice seedlings: case of phosphorus deficiency. Plant Prod Sci 8:145–151

    Article  CAS  Google Scholar 

  • Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, Beveridge CA, Ghisalberti EL, Smith SM (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA 108:8897–8902

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Park MR, Baek S-H, de los Reyes BG, Yun SJ, Hasenstein KH (2012) Transcriptome profiling characterizes phosphate deficiency effects on carbohydrate metabolism in rice leaves. J Plant Physiol 169:193–205

    Article  CAS  PubMed  Google Scholar 

  • Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Yoneyama K, Nogue F, Rameau C (2011) Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138:1531–1539

    Article  CAS  PubMed  Google Scholar 

  • Raghothama KG (2000) Phosphate transport and signaling. Curr Opin Plant Biol 3:182–187

    Article  CAS  PubMed  Google Scholar 

  • Roberts IN, Caputo C, Criado MV, Funk C (2012) Senescence-associated proteases in plants. Physiol Plant 145:130–139

    Article  CAS  PubMed  Google Scholar 

  • Seto Y, Kameoka H, Yamaguchi S, Kyozuka J (2012) Recent advances in strigolactone research: chemical and biological aspects. Plant Cell Physiol 53:1843–1853

    Article  CAS  PubMed  Google Scholar 

  • Seto Y, Sado A, Asami K, Hanada A, Umehara M, Akiyama K, Yamaguchi S (2014) Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc Natl Acad Sci USA 111:1640–1645

    Article  CAS  PubMed  Google Scholar 

  • Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ (2005) The Decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17:746–759

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Umehara M (2011) Strigolactone, a key regulator of nutrient allocation in plants. Plant Biotechnol 28:429–437

    Article  CAS  Google Scholar 

  • Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200

    Article  CAS  PubMed  Google Scholar 

  • Umehara M, Hanada A, Magome H, Takeda-Kamiya N, Yamaguchi S (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 51:1118–1126

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Woo HR, Chung KM, Park JH, Oh SA, Ahn T, Hong SH, Jang SK, Nam HG (2001) ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13:1779–1790

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yan H, Saika H, Maekawa M, Takamure I, Tsutsumi N, Kyozuka J, Nakazono M (2007) Rice tillering dwarf mutant dwarf3 has increased leaf longevity during darkness-induced senescence or hydrogen peroxide-induced cell death. Genes Genet Syst 82:361–366

    Article  CAS  PubMed  Google Scholar 

  • Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007a) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125–132

    Article  CAS  PubMed  Google Scholar 

  • Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007b) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225:1031–1038

    Article  CAS  PubMed  Google Scholar 

  • Yoneyama K, Xie X, Kim HI, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235:1197–1207

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yoneyama K, Xie X, Kisugi T, Nomura T, Yoneyama K (2013) Nitrogen and phosphorus fertilization negatively affects strigolactone production and exudation in sorghum. Planta 238:885–894

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S, Kameoka H, Tempo M, Akiyama K, Umehara M, Yamaguchi S, Hayashi H, Kyozuka J, Shirasu K (2012) The D3 F-box protein is a key component in host strigolactone responses essential for arbuscular mycorrhizal symbiosis. New Phytol 196:1208–1216

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Junko Kyozuka (University of Tokyo) for providing seeds of the rice d mutants, and Jun Kajino and Keisuke Kato (Toyo University) for their technical assistance. This work was supported by Grants-in-Aid for Scientific Research on Innovative Area and for Scientific Research (B) from Japan’s Ministry of Education, Culture, Sports, Science and Technology (Nos. 23119523 and 23370025), by the Inoue Enryo Memorial Foundation for Promoting Sciences from Toyo University, and by the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry (PROBRAIN).

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Correspondence to Mikihisa Umehara.

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Yamada, Y., Furusawa, S., Nagasaka, S. et al. Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 240, 399–408 (2014). https://doi.org/10.1007/s00425-014-2096-0

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