Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs

Significance Strigolactones are a new class of plant hormones regulating plant shoot and root architecture in response to the environment. Also present in root exudates, strigolactones stimulate the germination of parasitic plant seeds. This report describes a genomic polymorphism—associated with the Indica/Japonica subspecies divide in rice that has a major impact on the biosynthesis of strigolactones, plant tillering, and germination of the parasitic plant Striga hermonthica—consisting of the deletion of two strigolactone biosynthetic genes orthologous to Arabidopsis MAX1. Both of these genes rescued the Arabidopsis max1-1 highly branched mutant phenotype and increased the strigolactone level when overexpressed in the Indica rice variety Bala. This finding is of great interest for plant physiologists, plant evolutionary biologists, and breeders. Rice (Oryza sativa) cultivar Azucena—belonging to the Japonica subspecies—exudes high strigolactone (SL) levels and induces high germination of the root parasitic plant Striga hermonthica. Consistent with the fact that SLs also inhibit shoot branching, Azucena is a low-tillering variety. In contrast, Bala, an Indica cultivar, is a low-SL producer, stimulates less Striga germination, and is highly tillered. Using a Bala × Azucena F6 population, a major quantitative trait loci—qSLB1.1—for the exudation of SL, tillering, and induction of Striga germination was detected on chromosome 1. Sequence analysis of the corresponding locus revealed a rearrangement of a 51- to 59-kbp stretch between 28.9 and 29 Mbp in the Bala genome, resulting in the deletion of two cytochrome P450 genes—SLB1 and SLB2—with high homology to the Arabidopsis SL biosynthesis gene, MAX1. Both rice genes rescue the Arabidopsis max1-1 highly branched mutant phenotype and increase the production of the SL, ent-2′-epi-5-deoxystrigol, when overexpressed in Bala. Furthermore, analysis of this region in 367 cultivars of the publicly available Rice Diversity Panel population shows that the rearrangement at this locus is a recurrent natural trait associated with the Indica/Japonica divide in rice.

[1]  Paul R Zurek,et al.  3D phenotyping and quantitative trait locus mapping identify core regions of the rice genome controlling root architecture , 2013, Proceedings of the National Academy of Sciences.

[2]  Ottoline Leyser,et al.  A Role for MORE AXILLARY GROWTH1 (MAX1) in Evolutionary Diversity in Strigolactone Signaling Upstream of MAX21[C][W][OA] , 2013, Plant Physiology.

[3]  Yoshihiro Kawahara,et al.  Rice Annotation Project Database (RAP-DB): An Integrative and Interactive Database for Rice Genomics , 2013, Plant & cell physiology.

[4]  K. Akiyama,et al.  Confirming Stereochemical Structures of Strigolactones Produced by Rice and Tobacco , 2012, Molecular plant.

[5]  D. Schwartz,et al.  Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data , 2013, Rice.

[6]  R. Newcomb,et al.  DAD2 Is an α/β Hydrolase Likely to Be Involved in the Perception of the Plant Branching Hormone, Strigolactone , 2012, Current Biology.

[7]  H. Bouwmeester,et al.  Strigolactones affect development in primitive plants. The missing link between plants and arbuscular mycorrhizal fungi? , 2012, The New phytologist.

[8]  P. Beyer,et al.  The Path from β-Carotene to Carlactone, a Strigolactone-Like Plant Hormone , 2012, Science.

[9]  Joanne L. Simons,et al.  The Expression of Petunia Strigolactone Pathway Genes is Altered as Part of the Endogenous Developmental Program , 2012, Front. Plant Sci..

[10]  H. Bouwmeester,et al.  Pre-attachment Striga hermonthica resistance of New Rice for Africa (NERICA) cultivars based on low strigolactone production. , 2011, The New phytologist.

[11]  T. Bisseling,et al.  IPD3 controls the formation of nitrogen-fixing symbiosomes in pea and Medicago Spp. , 2011, Molecular plant-microbe interactions : MPMI.

[12]  H. Bouwmeester,et al.  Genetic variation in strigolactone production and tillering in rice and its effect on Striga hermonthica infection , 2011, Planta.

[13]  Mark H. Wright,et al.  Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa , 2011, Nature communications.

[14]  Keyan Zhao,et al.  Genetic Architecture of Aluminum Tolerance in Rice (Oryza sativa) Determined through Genome-Wide Association Analysis and QTL Mapping , 2011, PLoS genetics.

[15]  Ottoline Leyser,et al.  Signal integration in the control of shoot branching , 2011, Nature Reviews Molecular Cell Biology.

[16]  H. Bouwmeester,et al.  Strigolactones and root infestation by plant-parasitic Striga, Orobanche and Phelipanche spp. , 2011, Plant science : an international journal of experimental plant biology.

[17]  O. Leyser,et al.  Strigolactones Are Transported through the Xylem and Play a Key Role in Shoot Architectural Response to Phosphate Deficiency in Nonarbuscular Mycorrhizal Host Arabidopsis1[C][W][OA] , 2010, Plant Physiology.

[18]  H. Bouwmeester,et al.  Physiological Effects of the Synthetic Strigolactone Analog GR24 on Root System Architecture in Arabidopsis: Another Belowground Role for Strigolactones?1[C][W][OA] , 2010, Plant Physiology.

[19]  Shinjiro Yamaguchi,et al.  Contribution of Strigolactones to the Inhibition of Tiller Bud Outgrowth under Phosphate Deficiency in Rice , 2010, Plant & cell physiology.

[20]  C. Bustamante,et al.  Genomic Diversity and Introgression in O. sativa Reveal the Impact of Domestication and Breeding on the Rice Genome , 2010, PloS one.

[21]  Richard Durbin,et al.  Fast and accurate long-read alignment with Burrows–Wheeler transform , 2010, Bioinform..

[22]  G. Bécard,et al.  Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis , 2010, Planta.

[23]  Y. Kapulnik,et al.  Strigolactones’ Effect on Root Growth and Root-Hair Elongation May Be Mediated by Auxin-Efflux Carriers , 2010, Journal of Plant Growth Regulation.

[24]  Shinjiro Yamaguchi,et al.  d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. , 2009, Plant & cell physiology.

[25]  C. Bustamante,et al.  Evolutionary History of GS3, a Gene Conferring Grain Length in Rice , 2009, Genetics.

[26]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[27]  Chris Parker,et al.  Observations on the current status of Orobanche and Striga problems worldwide. , 2009, Pest management science.

[28]  Zhen Su,et al.  DWARF27, an Iron-Containing Protein Required for the Biosynthesis of Strigolactones, Regulates Rice Tiller Bud Outgrowth[W][OA] , 2009, The Plant Cell Online.

[29]  K. Ozawa Establishment of a high efficiency Agrobacterium-mediated transformation system of rice (Oryza sativa L.). , 2009, Plant science : an international journal of experimental plant biology.

[30]  A. Price,et al.  Mapping of quantitative trait loci for seminal root morphology and gravitropic response in rice , 2009, Euphytica.

[31]  A. Price,et al.  A study on the susceptibility of rice cultivars to Striga hermonthica and mapping of Striga tolerance quantitative trait loci in rice. , 2008, The New phytologist.

[32]  Jean-Charles Portais,et al.  Strigolactone inhibition of shoot branching , 2008, Nature.

[33]  Y. Kamiya,et al.  Inhibition of shoot branching by new terpenoid plant hormones , 2008, Nature.

[34]  S. Mccouch,et al.  New insights into the history of rice domestication. , 2007, Trends in genetics : TIG.

[35]  Hitoshi Sakakibara,et al.  DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. , 2007, The Plant journal : for cell and molecular biology.

[36]  C. Bustamante,et al.  Global Dissemination of a Single Mutation Conferring White Pericarp in Rice , 2007, PLoS genetics.

[37]  H. Bouwmeester,et al.  Rhizosphere communication of plants, parasitic plants and AM fungi. , 2007, Trends in plant science.

[38]  Qi Xie,et al.  The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. , 2006, The Plant journal : for cell and molecular biology.

[39]  J. Slate,et al.  A novel form of resistance in rice to the angiosperm parasite Striga hermonthica. , 2006, The New phytologist.

[40]  H. Bouwmeester,et al.  The Strigolactone Germination Stimulants of the Plant-Parasitic Striga and Orobanche spp. Are Derived from the Carotenoid Pathway1 , 2005, Plant Physiology.

[41]  K. Akiyama,et al.  Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi , 2005, Nature.

[42]  C. Turnbull,et al.  MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. , 2005, Developmental cell.

[43]  O. Leyser,et al.  MAX3/CCD7 Is a Carotenoid Cleavage Dioxygenase Required for the Synthesis of a Novel Plant Signaling Molecule , 2004, Current Biology.

[44]  D. Mackill,et al.  Locating genes associated with root morphology and drought avoidance in rice via linkage to molecular markers , 1995, Theoretical and Applied Genetics.

[45]  A. Gleave A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome , 1992, Plant Molecular Biology.

[46]  P. Reich,et al.  Long-term increase in nitrogen supply alters above- and below-ground ectomycorrhizal communities and increases the dominance of Russula spp. in a temperate oak savanna. , 2003, The New phytologist.

[47]  C. Beveridge,et al.  MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. , 2003, Genes & development.

[48]  M. Osaki,et al.  Expression of the OsPI1 gene, cloned from rice roots using cDNA microarray, rapidly responds to phosphorus status , 2003 .

[49]  O. Clarenz,et al.  Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. , 2003, Genes & development.

[50]  A. Price,et al.  Upland rice grown in soil-filled chambers and exposed to contrasting water-deficit regimes: II. Mapping quantitative trait loci for root morphology and distribution , 2002 .

[51]  A. Price,et al.  A combined RFLP and AFLP linkage map of upland rice (Oryza sativa L.) used to identify QTLs for root-penetration ability , 2000, Theoretical and Applied Genetics.

[52]  M. Press,et al.  Infection time and density influence the response of sorghum to the parasitic angiosperm Striga hermonthica. , 1999, The New phytologist.

[53]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[54]  C. Chu,et al.  ESTABLISHMENT OF AN EFFICIENT MEDIUM FOR ANTHER CULTURE OF RICE THROUGH COMPARATIVE EXPERIMENTS ON THE NITROGEN SOURCES , 1975 .

[55]  R. Miller,et al.  Nutrient requirements of suspension cultures of soybean root cells. , 1968, Experimental cell research.