The importance of strigolactone transport regulation for symbiotic signaling and shoot branching

AbstractMain conclusionThis review presents the role of strigolactone transport in regulating plant root and shoot architecture, plant-fungal symbiosis and the crosstalk with several phytohormone pathways. The authors, based on their data and recently published results, suggest that long-distance, as well local strigolactone transport might occur in a cell-to-cell manner rather than via the xylem stream. Strigolactones (SLs) are recently characterized carotenoid-derived phytohormones. They play multiple roles in plant architecture and, once exuded from roots to soil, in plant-rhizosphere interactions. Above ground SLs regulate plant developmental processes, such as lateral bud outgrowth, internode elongation and stem secondary growth. Below ground, SLs are involved in lateral root initiation, main root elongation and the establishment of the plant-fungal symbiosis known as mycorrhiza. Much has been discovered on players and patterns of SL biosynthesis and signaling and shown to be largely conserved among different plant species, however little is known about SL distribution in plants and its transport from the root to the soil. At present, the only characterized SL transporters are the ABCG protein PLEIOTROPIC DRUG RESISTANCE 1 from Petunia axillaris (PDR1) and, in less detail, its close homologue from Nicotiana tabacum PLEIOTROPIC DRUG RESISTANCE 6 (PDR6). PDR1 is a plasma membrane-localized SL cellular exporter, expressed in root cortex and shoot axils. Its expression level is regulated by its own substrate, but also by the phytohormone auxin, soil nutrient conditions (mainly phosphate availability) and mycorrhization levels. Hence, PDR1 integrates information from nutrient availability and hormonal signaling, thus synchronizing plant growth with nutrient uptake. In this review we discuss the effects of PDR1 de-regulation on plant development and mycorrhization, the possible cross-talk between SLs and other phytohormone transporters and finally the need for SL transporters in different plant species.

[1]  B. Janssen,et al.  Regulation of axillary shoot development. , 2014, Current opinion in plant biology.

[2]  K. Dixon,et al.  A Compound from Smoke That Promotes Seed Germination , 2004, Science.

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

[4]  H. Bouwmeester,et al.  A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching , 2012, Nature.

[5]  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.

[6]  M. Strnad,et al.  Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins , 2014, Nature Communications.

[7]  Haiyang Wang,et al.  D14-SCFD3-dependent degradation of D53 regulates strigolactone signaling , 2013, Nature.

[8]  Ben Scheres,et al.  Polar PIN Localization Directs Auxin Flow in Plants , 2006, Science.

[9]  J. Chen,et al.  The jasmonate-responsive GTR1 transporter is required for gibberellin-mediated stamen development in Arabidopsis , 2015, Nature Communications.

[10]  C. Beveridge,et al.  Sugar demand, not auxin, is the initial regulator of apical dominance , 2014, Proceedings of the National Academy of Sciences.

[11]  T. Kiba,et al.  Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin , 2014, Proceedings of the National Academy of Sciences.

[12]  M. Hofmann,et al.  Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. , 2014, Nature chemical biology.

[13]  M. E. Light,et al.  Isolation of the major germination cue from plant-derived smoke , 2004 .

[14]  J. Friml,et al.  PIN-Dependent Auxin Transport: Action, Regulation, and Evolution , 2015, Plant Cell.

[15]  T. Teichmann,et al.  Shaping plant architecture , 2015, Front. Plant Sci..

[16]  Hui Shen,et al.  The F-Box Protein MAX2 Functions as a Positive Regulator of Photomorphogenesis in Arabidopsis1[C][W][OA] , 2007, Plant Physiology.

[17]  J. Friml,et al.  Asymmetric Localizations of the ABC Transporter PaPDR1 Trace Paths of Directional Strigolactone Transport , 2015, Current Biology.

[18]  K. Akiyama,et al.  Structural Requirements of Strigolactones for Hyphal Branching in AM Fungi , 2010, Plant & cell physiology.

[19]  Zeng-Fu Xu,et al.  Gibberellin Promotes Shoot Branching in the Perennial Woody Plant Jatropha curcas , 2015, Plant & cell physiology.

[20]  H. Ueda,et al.  Strigolactone Regulates Leaf Senescence in Concert with Ethylene in Arabidopsis1 , 2015, Plant Physiology.

[21]  O. Leyser,et al.  Strigolactone Can Promote or Inhibit Shoot Branching by Triggering Rapid Depletion of the Auxin Efflux Protein PIN1 from the Plasma Membrane , 2013, PLoS biology.

[22]  Mark T Waters,et al.  The Arabidopsis Ortholog of Rice DWARF27 Acts Upstream of MAX1 in the Control of Plant Development by Strigolactones1[C][W][OA] , 2012, Plant Physiology.

[23]  Y. Kapulnik,et al.  Influx and Efflux of Strigolactones Are Actively Regulated and Involve the Cell-Trafficking System. , 2015, Molecular plant.

[24]  A. Fernie,et al.  SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. , 2009, The Plant journal : for cell and molecular biology.

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

[26]  Ottoline Leyser,et al.  Hormonally controlled expression of the Arabidopsis MAX4 shoot branching regulatory gene. , 2005, The Plant journal : for cell and molecular biology.

[27]  Atsushi Hanada,et al.  FINE CULM1 (FC1) Works Downstream of Strigolactones to Inhibit the Outgrowth of Axillary Buds in Rice , 2010, Plant & cell physiology.

[28]  Q. Xia,et al.  Cloning and characterization of a novel Nicotiana tabacum ABC transporter involved in shoot branching. , 2015, Physiologia plantarum.

[29]  R. Koide,et al.  Can hypodermal passage cell distribution limit root penetration by mycorrhizal fungi? , 2008, The New phytologist.

[30]  K. Dixon,et al.  Identification of alkyl substituted 2H-furo[2,3-c]pyran-2-ones as germination stimulants present in smoke. , 2009, Journal of agricultural and food chemistry.

[31]  K. Yoneyama,et al.  Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites , 2007, Planta.

[32]  C. Beveridge,et al.  Interactions between Auxin and Strigolactone in Shoot Branching Control1[C][OA] , 2009, Plant Physiology.

[33]  H. Bouwmeester,et al.  Fine-tuning regulation of strigolactone biosynthesis under phosphate starvation , 2008, Plant signaling & behavior.

[34]  H. Bouwmeester,et al.  The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. , 2012, The New phytologist.

[35]  Jean-Michel Claverie,et al.  Phylogeny.fr: robust phylogenetic analysis for the non-specialist , 2008, Nucleic Acids Res..

[36]  Ecological relevance of strigolactones in nutrient uptake and other abiotic stresses, and in plant-microbe interactions below-ground , 2015, Plant and Soil.

[37]  S. Al‐Babili,et al.  Strigolactones, a novel carotenoid-derived plant hormone. , 2015, Annual review of plant biology.

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

[39]  Caitlin E. Conn,et al.  Evidence that KARRIKIN-INSENSITIVE2 (KAI2) Receptors may Perceive an Unknown Signal that is not Karrikin or Strigolactone , 2016, Front. Plant Sci..

[40]  Steven M. L. Smith,et al.  SUPPRESSOR OF MORE AXILLARY GROWTH2 1 Controls Seed Germination and Seedling Development in Arabidopsis1[W][OPEN] , 2013, Plant Physiology.

[41]  G. Krouk,et al.  ABA transport and transporters. , 2013, Trends in plant science.

[42]  Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency , 2014, Planta.

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

[44]  Youngsook Lee,et al.  The role of ABCG-type ABC transporters in phytohormone transport , 2015, Biochemical Society transactions.

[45]  S. Assmann,et al.  PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid , 2010, Proceedings of the National Academy of Sciences.

[46]  O. Leyser,et al.  Strigolactone signalling: standing on the shoulders of DWARFs. , 2014, Current opinion in plant biology.

[47]  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.

[48]  M. Kumar,et al.  Strigolactone analog GR24 triggers changes in PIN2 polarity, vesicle trafficking and actin filament architecture. , 2014, The New phytologist.

[49]  S. Rochange,et al.  Strigolactones contribute to shoot elongation and to the formation of leaf margin serrations in Medicago truncatula R108. , 2015, Journal of experimental botany.

[50]  C. Beveridge,et al.  Dynamics of strigolactone function and shoot branching responses in Pisum sativum. , 2013, Molecular plant.

[51]  O. Leyser,et al.  SMAX1-LIKE/D53 Family Members Enable Distinct MAX2-Dependent Responses to Strigolactones and Karrikins in Arabidopsis , 2015, Plant Cell.

[52]  Wenjiao Zhu,et al.  Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. , 2013, Developmental cell.

[53]  M. Wall,et al.  Germination of Witchweed (Striga lutea Lour.): Isolation and Properties of a Potent Stimulant , 1966, Science.

[54]  C. Kuhlemeier,et al.  Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. , 2010, The Plant journal : for cell and molecular biology.

[55]  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.

[56]  Haiyang Wang,et al.  Corrigendum: D14–SCFD3-dependent degradation of D53 regulates strigolactone signalling , 2016, Nature.

[57]  Da Luo,et al.  The Pea TCP Transcription Factor PsBRC1 Acts Downstream of Strigolactones to Control Shoot Branching1[W] , 2011, Plant Physiology.

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

[59]  Seung-Hyun Park,et al.  Molecular mechanism of strigolactone perception by DWARF14 , 2013, Nature Communications.

[60]  T. Kuyper,et al.  Colonization by Arbuscular Mycorrhizal Fungi of Sorghum Leads to Reduced Germination and Subsequent Attachment and Emergence of Striga hermonthica , 2007, Plant signaling & behavior.

[61]  Fusuo Zhang,et al.  Phosphorus sustains life , 2011, Plant and Soil.

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

[63]  C. Rameau,et al.  Strigolactone biosynthesis and signaling in plant development , 2015, Development.

[64]  Patrick Mulder,et al.  Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. , 2008, The New phytologist.

[65]  J. B. Reid,et al.  Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. , 2013, Molecular plant.

[66]  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.

[67]  O. Leyser,et al.  Strigolactones and the control of plant development: lessons from shoot branching. , 2014, The Plant journal : for cell and molecular biology.

[68]  K. Akiyama,et al.  Strigolactones are transported from roots to shoots, although not through the xylem , 2015 .

[69]  Shinjiro Yamaguchi,et al.  Carlactone is an endogenous biosynthetic precursor for strigolactones , 2014, Proceedings of the National Academy of Sciences.

[70]  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.

[71]  Q. Qian,et al.  DWARF 53 acts as a repressor of strigolactone signalling in rice , 2013, Nature.

[72]  Shinjiro Yamaguchi,et al.  Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro , 2014, Proceedings of the National Academy of Sciences.

[73]  T. Brutnell,et al.  Tillering in the sugary1 sweet corn is maintained by overriding the teosinte branched1 repressive signal , 2015, Plant signaling & behavior.

[74]  J. Rolcik,et al.  Sucrose is an early modulator of the key hormonal mechanisms controlling bud outgrowth in Rosa hybrida , 2015, Journal of experimental botany.

[75]  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.

[76]  K. Yoneyama,et al.  Feedback-Regulation of Strigolactone Biosynthetic Genes and Strigolactone-Regulated Genes in Arabidopsis , 2009, Bioscience, biotechnology, and biochemistry.