Strigolactones inhibit shoot. branching. In mutant plants unable to make SLs, many more shoot branches grow out

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1 The Plant Cell, ctober H H STRIGLACTNES Strigolactones inhibit shoot branching Wild type -deficient In mutant plants unable to make s, many more shoot branches grow out What is the connection between: Shoot branching Root parasitism, and Root symbiosis? Image courtesy RIKEN Image courtesy RIKEN Strigolactones contribute to a devastating form of plant parasitism Strigolactones promote beneficial symbiotic interactions Three seemingly independent topics converged on s Striga hermonthica Striga are parasitic plants that are the single largest biotic cause of reduced crop yields throughout Africa (> $1 billion per year in yield losses) Striga germination is induced by strigolactones produced by host plant roots Host Root parasites Striga s promotes the symbiotic association with AM fungi. This symbiosis occurs in 8% of land plants and helps them assimilate nutrients from the soil Arbuscular is derived from Latin for tree (arbor). Mycorrhiza means fungus root Symbiotic rigins of plant / mycorrhizal symbiosis > 46 mya Evolution of plant parasitism 18s - Recognition of AM fungus / plant symbiosis 18s - Host plant factor required for parasitic seed germination 19s - Role of auxin in shoot branching described Search for branching factor s 197s Purification and characterization of strigol from roots 199s 2s Branching mutants described in petunia, pea, Arabidopsis and rice 25: Strigolactones promote hyphal branching 28: Strigolactones inhibit shoot branching Image source: USDA APHIS PPQ Archive Image courtesy of Mark Brundrett Strigolactones (s) regulate seemingly unrelated events Strigolatones promote germination of parasitic Striga seeds Strigolactones have been co-opted for various functions s inhibit shoot branching s promote associations with arbuscular mycorrhizal (AM) fungi s promote germination of parasitic Striga plants Host Root Striga Their common name is witchweed because the plants appear to be cursed. Typically Striga infestation causes reductions in crop yields of 5 1% s ancestral function may have been communication between individuals of the same species (as pheromones or quormones) Root parasite s now contribute to communication within an individual (as hormones), and between individuals of different species (and kingdoms) (as allelochemicals) Striga-infested maize field Image source USDA APHIS PPQ Archive See for example Tsuchiya, Y. and McCourt, P. (212). Strigolactones as small molecule communicators. Mol. BioSyst. 8: ; Delaux, P.-M., et al., (212). rigin of strigolactones in the green lineage. New Phytol. 195: ; Proust, H., et al., (211). Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development. 138:

2 The Plant Cell, ctober Reprinted from Booker, J., et al. (24). MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr. Biol. 14: with permission from Elsevier; Morris, S.E., et al. (21). Mutational analysis of branching in pea. Evidence that Rms1 and Rms5 regulate the same novel signal. Plant Physiol. 126: ; Ishikawa, S., et al. (25). Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol. 46: by permission of the Japanese Society of Plant Physiologists. Simons, J.L., et al. (27). Analysis of the DECREASED APICAL DMINANCE genes of petunia in the control of axillary branching. Plant Physiol. 143: Lecture utline Synthesis Perception and signaling Strigolactones in wholeplant processes: Shoot branching ther developmental effects Moss colony growth Symbiosis Germination Towards the elimination of Striga parasitism The stimulator of Striga germination derives from the carotenoid pathway Carotenoiddeficient mutants do not make germination stimulator mutant mutant Through the use of maize mutants and enzyme inhibitors, carotenoids were demonstrated to be the precursors of s fluridone -carotene MEP pathway GGPP phytoene 5-deoxystrigol D27 encodes an Fe-binding enzyme necessary for synthesis Strigolactones are detected in Wild-type exudates of wild-type but not d27 roots (Shiokari) d27 Standard Wild-type exudate d27 exudate The rice D27 is a β- carotene-9-isomerase also found in other plants Image source USDA APHIS PPQ Archive Matusova, R., Rani, K., Verstappen, F.W.A., Franssen, M.C.R., Beale, M.H., and Bouwmeester, H.J. (25). The strigolactone germination stimulants of the plant-parasitic Striga and robanche spp. are derived from the carotenoid pathway. Plant Physiol. 139: Lin, H., Wang, R., Qian, Q., Yan, M., Meng, X., Fu, Z., Yan, C., Jiang, B., Su, Z., Li, J. and Wang, Y. (29). DWARF27, an ironcontaining protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell. 21: Synthesis and transport In a search for stimulators of Striga germination, strigolactones were purified from cotton roots in 1966 and the chemical structure determined in 1972 Cook, C.E., Whichard, L.P., Turner, B., Wall, M.E., and Egley, G.H. (1966). Germination of witchweed (Striga lutea Lour.): Isolation and properties of a potent stimulant. Science 154: ; Reprinted with permission from Cook, C.E., Whichard, L.P., Wall, M., Egley, G.H., Coggon, P., Luhan, P.A., and McPhail, A.T. (1972). Germination stimulants. II. Structure of strigol, a potent seed germination stimulant for witchweed (Striga lutea). J. Am. Chem. Soc. 94: Genes involved in biosynthesis were identified by genetic methods max3 rms5 Strigolactone-deficient mutants in Arabidopsis, pea, rice and petunia show similar short, branchy phenotypes dad3 The MRE AXILLARY GRH3 (MAX3), RAMSUS5 (RMS5), DWARF17 (D17) and DECREASED APICAL DMINANCE3 (DAD3) genes all encode a carotenoid cleavage dioxygenase (CCD7) Rice biosynthesis mutants are rescued by exogenous D17 D1 d1 and d17 are rescued by exogenous 1st leaf tiller 2nd leaf tiller d1 d17 d1 d17 Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (28). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-2; 1 cm 1 cm Control GR24 (1 µm) (GR24 is a synthetic ) Strigolactones (s) are a small family of compounds biosynthesis pathway Arabidopsis biosynthesis mutants are rescued by There are many naturally occurring s, derived from 5-deoxystrigol D27 (β-carotene-9-isomerase) These MAX3, D17, RMS5, DAD3: CCD7 reactions occur in the plastid MAX4, D1,RMS1, DAD1: CCD8 carlactone MAX3 MAX4 Control 5-Deoxystrigol SYNTHESIS MAX; Arabidopsis D; rice RMS; pea DAD; petunia MAX1 (P45) STRIGLACTNES MAX1 max1 max3 max4 GR24 (5 µm) Reprinted from Humphrey, A.J., and Beale, M.H. (26). Strigol: Biogenesis and physiological activity. Phytochemistry 67: with permission from Elsevier; See also Boyer, F.D., et al.. and Rameau, C. (212). Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: molecule design for shoot branching. Plant Physiol. 159: Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (28). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: ; Seto Y, Kameoka H, Yamaguchi S, Kyozuka J. (212) Recent advances in strigolactone research: chemical and biological aspects. (in press). Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., Ghisla, S., Bouwmeester, H., Beyer, P., and Al-Babili, S. (212). The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science. 335: Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (28). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-2; Seto Y, Kameoka H, Yamaguchi S, Kyozuka J. (212) Recent advances in strigolactone research: chemical and biological aspects. (in press). 2

3 The Plant Cell, ctober Reprinted from Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., Turnbull, C., Srinivasan, M., Goddard, P., and Leyser,. (25). MAX1 encodes a cytochrome P45 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Developmental Cell 8: with permission from Elsevier. MAX1 encodes a P45 enzyme involved in shoot branching PDR1 has been identified as a strigolactone exporter Perception and signaling MAX1 max1 MAX1 is expressed throughout the plant, primarily in association with vascular tissues pdr1 Loss-of-function pdr1 mutant show: increased shoot branching decreased exudation of s decreased symbiotic interactions dad1 (=max4) s are present in pdr1 root extracts, but not prd1 exudates, supporting its role as a transporter pdr1 mutants are less colonized by, and stimulate less parasitic seed germination 2. D3 is an F-box protein that promotes interaction with the proteasome 3. The interaction between s, D14 1. D14 is an α/βfold hydrolase that and D3 leads to degradation of target proteins including D53 (SMAX) binds s Kretzschmar, T., Kohlen, W., Sasse, J., Borghi, L., Schlegel, M., Bachelier, J.B., Reinhardt, D., Bours, R., Bouwmeester, H.J. and Martinoia, E. (212). A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature. 483: Reprinted by permission from Macmillan Publishers Ltd: Zhou, F., et al and Wan, J. (213). D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 54: synthesis in root or shoot is sufficient to control shoot branching max3 max3 Grafts max3 Reciprocal grafts, in which wildtype tissue is either the root or scion, have normal phenotypes; this says that the branchcontrolling signal can be made in either tissue, and can move from root to shoot Scion Root The distribution of PDR1 is consistent with its roles in transport s are transported shootward and outward from the root 1. D14 is an α/β-fold hydrolase that binds s \ Genetic studies Loss-of-function d14 mutants are insensitive and show increased shoot branching; the orthologous gene in petunia is dad2 Biochemical studies D14 and DAD2 are α/β-fold hydrolases similar to the GID1 protein involved in gibberellin perception Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., Turnbull, C., Srinivasan, M., Goddard, P., and Leyser,. (25). MAX1 encodes a cytochrome P45 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Developmental Cell 8: Reprinted from Sasse, J., Simon, S., Gübeli, C., Liu, G.-W., Cheng, X., Friml, J., Bouwmeester, H., Martinoia, E. and Borghi, L. (215). Asymmetric localizations of the ABC transporter PaPDR1 trace paths of directional strigolactone transport. Curr. Biol. 25: and Ruyter-Spira, C., Al-Babili, S., van der Krol, S. and Bouwmeester, H. (213). The biology of strigolactones. Trends Plant Sci. 18: with permission from Elsevier. Arite, T., Umehara, M., Ishikawa, S., Hanada, A., Maekawa, M., Yamaguchi, S. and Kyozuka, J. (29). d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol. 5: ; Hamiaux, C., Drummond, R.S., Janssen, B.J., Ledger, S.E., Cooney, J.M., Newcomb, R.D. and Snowden, K.C. (212). DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol. 22: An intermediate between MAX4 and MAX1 action can move in the plant Synthesis and transport - summary The α/β-fold hydrolase D14/DAD2 cleaves STRIGLACTNES MAX4 MAX1 max1 max4 max4 max1 Carlactone is a good candidate as the mobile signalling molecule In this experiment mobile, grafttransmissible intermediate in synthesis is produced in max1 roots, and converted into in max4 shoots Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., Turnbull, C., Srinivasan, M., Goddard, P., and Leyser,. (25). MAX1 encodes a cytochrome P45 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Developmental Cell 8: ; Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., Ghisla, S., Bouwmeester, H., Beyer, P., and Al-Babili, S. (212). The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science. 335: s are derived from carotenoids; Early steps occur in D27 (β-carotene-9-isomerase) the plastids of root and shoot MAX3, RMS5, D17, DAD3 (CCD7) MAX4, RMS1, D1, DAD1 Carlactone is an (CCD8) intermediate (and may carlactone be a mobile signal) MAX1 MAX; Arabidopsis (P45) RMS; pea D; rice DAD; petunia STRIGLACTNES Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., Ghisla, S., Bouwmeester, H., Beyer, P., and Al- Babili, S. (212). The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science. 335: Hydrolysis Nakamura, H., Xue, Y.L., Miyakawa, T., Hou, F., Qin, H.M., Fukui, K., Shi, X., Ito, E., Ito, S., Park, S.H., Miyauchi, Y., Asano, A., Totsuka, N., Ueda, T., Tanokura, M., and Asami, T. (213). Molecular mechanism of strigolactone perception by DWARF14. Nat Commun. 4: Seto, Y., and Yamaguchi, S. (214). Strigolactone biosynthesis and perception. Curr. pin. Plant Biol. 21: 1-6 with permission from Elsevier. 3

4 The Plant Cell, ctober receptors D14/DAD2 are related to the KAI2 karrikin receptors D14 probably arose from a duplication of KAI2 before the evolution of seed plants In the presence of s, DAD2/D14 interacts with D3/MAX2 concentrationdependent interaction Model of signal transduction between DAD2 (D14) and MAX2 (D3) (D3) Model: Strigolactone promotes D14- SCF D3 -mediated degradation of the repressor D53 Karrikins are small molecules present in smoke that are structurally similar to s and can induce seed germination Protein interaction A current model is that s promote the interaction between DAD2/D14 receptor and MAX2/D3, leading to degradation of a signaling repressor The D53 protein is a signaling repressor. D53 degradation by the proteasome depends on interaction with the D14/DAD2 receptor bound to. D14- and D3/MAX2 intermediate interaction between the D53 repressor and the SCF complex. Note the similarity of this model with those for auxin, jasmonate, salicylate and gibberellin signalling In Arabidopsis, D14 degradation is induced by via a MAX2-dependent proteasome mechanism. Conn, C.E., Bythell-Douglas, R., Neumann, D., Yoshida, S., Whittington, B., Westwood, J.H., Shirasu, K., Bond, C.S., Dyer, K.A., and Nelson, D.C. (215). Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 349: Reprinted with permission from AAAS. Hamiaux, C., Drummond, R.S., Janssen, B.J., Ledger, S.E., Cooney, J.M., Newcomb, R.D. and Snowden, K.C. (212). DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol. 22: ;Nelson, D.C., Scaffidi, A., Dun, E.A., Waters, M.T., Flematti, G.R., Dixon, K.W., Beveridge, C.A., Ghisalberti, E.L. and Smith, S.M. (211). F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA. 18: Zhou, F., Lin, Q., Zhu, L., Ren, Y., Zhou, K., Shabek, N., Wu, F., Mao, H., Dong, W., Gan, L., Ma, W., Gao, H., Chen, J., Yang, C., Wang, D., Tan, J., Zhang, X., Guo, X., Wang, J., Jiang, L., Liu, X., Chen, W., Chu, J., Yan, C., Ueno, K., Ito, S., Asami, T., Cheng, Z., Wang, J., Lei, C., Zhai, H., Wu, C., Wang, H., Zheng, N., and Wan, J. (213). Reprinted by permission from Macmillan Publishers Ltd: D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 54: Parasitic Striga make highlysensitive receptors Karrikin signals are transduced in a similar manner as s Signaling summary The receptor gene family is amplified in Striga ShHTL7 encodes a highly sensitive receptor protein that confers germination sensitivity to s in vivo MAX2 is needed for and karrikin signaling By analogy to s, karrikinbinding to KAI2 could promote its interaction with MAX2 and the degradation of repressor proteins D14/DAD2 is an / hydrolyze that binds, allowing interactions with the F-box protein D3/MAX2 D3/MAX2 brings the SCF complex and E2 ubiquitin ligase to D53 for polyubiquitination, and further degradation by the proteasome D53 degradation leads to transcriptional activation of target genes From Toh, S., Holbrook-Smith, D., Stogios, P.J., nopriyenko,., Lumba, S., Tsuchiya, Y., Savchenko, A. and McCourt, P. (215). Structurefunction analysis identifies highly sensitive strigolactone receptors in Striga. Science. 35: Reprinted with permission from AAAS. Nelson, D.C., Scaffidi, A., Dun, E.A., Waters, M.T., Flematti, G.R., Dixon, K.W., Beveridge, C.A., Ghisalberti, E.L. and Smith, S.M. (211). F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA. 18: ; Waters, M.T., Nelson, D.C., Scaffidi, A., Flematti, G.R., Sun, Y.K., Dixon, K.W. and Smith, S.M. (212). Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development. 139: Reprinted by permission from Macmillan Publishers Ltd: Jiang, L., Liu, X., Xiong, G., Liu, H., Chen, F., Wang, L., Meng, X., Liu, G., Yu, H., Yuan, Y., Yi, W., Zhao, L., Ma, H., He, Y., Wu, Z., Melcher, K., Qian, Q., Xu, H.E., Wang, Y., and Li, J. (213). DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 54: D3, an F-box protein, promotes interaction with the proteasome Control Auxin receptor Jasmonate co-receptor 3. Genetic approaches identified D53/SMXLs in signalling Loss-of-function smax1 mutants suppress mutant phenotypes Gain-of-function dominant d53 mutants show a -resistant, branchy phenotype Strigolactones have diverse roles in the development of vascular plants and moss Strigolactones and whole-plant processes d3 GR24 MAX2, D3 and (1 µm) RMS4 encode F-box proteins related to those involved in auxin and jasmonate signaling SMAX = Suppressor of MAX2 This include positive and negative effects Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (28). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: Johnson, X., Brcich, T., Dun, E.A., Goussot, M., Haurogne, K., Beveridge, C.A., and Rameau, C. (26). Branching genes are conserved across species. Genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol. 142: Stanga, J.P., Smith, S.M., Briggs, W.R. and Nelson, D.C. (213). SUPPRESSR F MRE AXILLARY GRH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol. 163: Jiang, L., and Li, J. (213). DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 54: Reprinted by permission from Macmillan Publishers Ltd: Zhou, F. et al.,, and Wan, J. (213). D14- SCF D3 -dependent degradation of D53 regulates strigolactone signalling. Nature 54: Seto, Y., Kameoka, H., Yamaguchi, S., and Kyozuka, J. (212). Recent advances in strigolactone research: chemical and biological aspects. Plant Cell Physiol. 53: by permission of xford University Press. 4

5 The Plant Cell, ctober Reprinted from Bennett, T., Sieberer, T., Willett, B., Booker, J., Luschnig, C., and Leyser,. (26). The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr. Biol. 16: with permission from Elsevier; Crawford, S., Shinohara, N., Sieberer, T., Williamson, L., George, G., Hepworth, J., Müller, D., Domagalska, M.A., and Leyser,. (21). Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137: reproduced with permission. Strigolactones regulate shoot /root branching and nutrient responses mutants produce more shoot and root branches In nutrient deficiency, elevated s repress shoot branching and promote root hair elongation Axillary bud outgrowth is hormonally and environmentally responsive bud Auxin and s inhibit outgrowth Cytokinins (CKs) promote it Nutrient control of branching Phosphatestarved plants suppress shoot growth and enhance root growth +P P (Axillla means armpit) Reprinted from Brewer, P.B., Koltai, H., and Beveridge, C.A. (213). Diverse roles of strigolactones in plant development. Mol Plant. 6: with permission of Elsevier. McSteen, P. (29). Hormonal regulation of branching in grasses. Plant Physiol. 149: 46-55; Brewer, P.B., Dun, E.A., Ferguson, B.J., Rameau, C., and Beveridge, C.A. (29). Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol. 15: Strigolactones dampen polar auxin transport (PAT) effect on branching can occur via effects on polar auxin transport Phosphorous deficiency limits plant growth in much of the world Transported auxin In shoots, strigolactones promote internalization of PIN auxin efflux transporters, decreasing polar auxin transport + -P -P -P PIN -deficient plants show increased polar auxin transport Auxin 4 million tonnes per year of phosphate fertilizer is mined, transported, applied to farmlands, and in many cases run-off to contaminate lakes and rivers -P Shinohara, N., Taylor, C., and Leyser,. (213) Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 11: e Image courtesy CIMMYT; FA (28) How do strigolactones inhibit bud outgrowth? effects on shoot branching can also be auxin-independent Transcriptional targets of s include BRC1, a transcription factor that represses bud outgrowth epi-5ds (ng gfw -1 ) No. of outgrowing tillers Strigolactones suppress shoot branching in low phosphorous Strigolactone level Tillering 3rd tiller 2nd tiller 1st tiller Strigolactone synthesis is high and shoot branching is suppressed when phosphate availability is low P (µm) +P P Goulet, C. and Klee, H.J. (21). Climbing the branches of the strigolactones pathway one discovery at a time. Plant Physiol. 154: Brewer, P.B., Dun, E.A., Gui, R., Mason, M.G. and Beveridge, C.A. (215). Strigolactone inhibition of branching independent of polar auxin transport. Plant Physiol. 168: Umehara, M., Hanada, A., Magome, H., Takeda-Kamiya, N., and Yamaguchi, S. (21). Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol. 51:

6 The Plant Cell, ctober In the -deficient d1 mutant, branch outgrowth is independent of [P] Furthermore, under low [P], s enhance root branching Strigolactones stimulate auxindependent secondary growth epi-5ds (ng gfw -1 ) No. of outgrowing tillers Strigolactone level Tillering P (µm) 3rd tiller 2nd tiller 1st tiller Strigolactone level d1 (None Detected) P (µm) In wild-type plants grown with exogenous auxin, outgrowth of lateral roots is enhanced by s, in combination with auxin, may control plant architecture under nutrient limiting conditions Low P synthesis max1-1 mutants show decreased lateral and longitudinal extension of interfascicular cambium-derived tissues (ICD) Umehara, M., Hanada, A., Magome, H., Takeda-Kamiya, N., and Yamaguchi, S. (21). Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol. 51: Ruyter-spira, C., et al. (211) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: Another below-ground role for strigolactones? Plant Physiology. 155: Agusti, J., Herold, S., Schwarz, M., Sanchez, P., Ljung, K., Dun, E.A., Brewer, P.B., Beveridge, C.A., Sieberer, T., Sehr, E.M., and Greb, T. (211). Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl. Acad. Sci. USA. 18: Low [P] induces -related gene expression in shoots and roots D27 (β-carotene-9-isomerase) MAX3/D17 (CCD7) MAX4/D1 (CCD8) MAX1 (P45) carotenoid carlactone Umehara, M., Hanada, A., Magome, H., Takeda-Kamiya, N., and Yamaguchi, S. (21). Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol. 51: These interlocking networks provide for local and systemic responses Low auxin Low High CK For example, hormone crosstalks coordinate shoot s development in response to nitrogen and phosphate limitation High bud outgrowth High auxin High Low CK Low bud outgrowth de Jong, M., George, G., ngaro, V., Williamson, L., Willetts, B., Ljung, K., McCulloch, H., and Leyser,. (214). Auxin and strigolactone signaling are required for modulation of Arabidopsis shoot branching by nitrogen supply. Plant Physiol. 166: Strigolactones regulate rice shoot gravitropism via auxin The lazy la mutant is deficient in lateral auxin distribution The sol1 mutant (suppressor of lazy), is a loss-offunction mutant of the F-box protein D3. deficient mutants have enhanced shoot gravitropism, perhaps due to increased auxin synthesis Sang, D., Chen, D., Liu, G., Liang, Y., Huang, L., Meng, X., Chu, J., Sun, X., Dong, G., Yuan, Y., Qian, Q., Li, J. and Wang, Y. (214). Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis. Proc. Natl. Acad. Sci. USA. 111: Low [P] lowers branch outgrowth in Arabidopsis, dependent on s Strigolactones suppress development of adventitious roots A. mutants of Arabidopsis show enhanced development of adventitious roots. B. Development of adventitious roots is supressed in wild-type and mutant with application in a dosedependent manner. Strigolactones stimulate leaf senescence mutants show delayed leaf senescence in petunia and Arabidopsis Exogenous s accelerate senescence Col- max4-1 Low P synthesis A. mutants of pea also show enhanced development of adventitious roots. B-C. Cuttings of wild-type (B) show development of less adventitious roots than the rms5 synthesis mutant (C). Kohlen, W., et al. (211) 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: Rasmussen, A., Mason, M.G., De Cuyper, C., Brewer, P.B., Herold, S., Agusti, J., Geelen, D., Greb, T., Goormachtig, S., Beeckman, T. and Beveridge, C.A. (212). Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol. 158: Reprinted from Hamiaux, C., Drummond, R.S., Janssen, B.J., Ledger, S.E., Cooney, J.M., Newcomb, R.D. and Snowden, K.C. (212). DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol. 22: , with permission from Elsevier. Snowden, K.C., Simkin, A.J., Janssen, B.J., Templeton, K.R., Loucas, H.M., Simons, J.L., Karunairetnam, S., Gleave, A.P., Clark, D.G., and Klee, H.J. (25). The Decreased apical dominance1/petunia hybrida CARTENID CLEAVAGE DIXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17: ; Ueda, H. and Kusaba, M. (215). Strigolactone regulates leaf senescence in concert with ethylene in Arabidopsis. Plant Physiol. doi:1.114/pp

7 The Plant Cell, ctober Ha, C.V., Leyva-González, M.A., sakabe, Y., Tran, U.T., Nishiyama, R., Watanabe, Y., Tanaka, M., Seki, M., Yamaguchi, S., Dong, N.V., Yamaguchi-Shinozaki, K., Shinozaki, K., Herrera-Estrella, L., and Tran, L.S. (214). Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci USA. 111: See Ruyter-Spira, C. and Bouwmeester, H. (212). Strigolactones affect development in primitive plants. The missing link between plants and arbuscular mycorrhizal fungi? New Phytologist. 195: Delaux, P.M., Xie, X., Timme, R.E., Puech- Pages, V., Dunand, C., Lecompte, E., Delwiche, C.F., Yoneyama, K., Becard, G. and Sejalon-Delmas, N. (212). rigin of strigolactones in the green lineage. New Phytol. 195: Tirithel; Christian Fischer Reprinted from Smith, Steven M. and Waters, Mark T. (212). Strigolactones: Destructiondependent perception? Curr. Biol. 22: R924-R927, with permission from Elsevier. Courtesy of K. Yoneyama and adapted from Yoneyama, K., Xie, X., Kusumoto, D., Sekimoto, H., Sugimoto, Y., Takeuchi, Y., and Yoneyama, K. (27). 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: Strigolactone mutants are more sensitive to abiotic stress control drought Model s are diffusible signals that reveal moss density When perceive s, they initiate symbiosis with the host plant These results suggest that strigolactones play a positive role in abiotic stress tolerance signals repress growth ccd8 N signal, no growth repression moss at periphery send signal, ccd8 moss in center perceives it and restricts growth Reproduced with permission from Proust, H., Hoffmann, B., Xie, X., Yoneyama, K., Schaefer, D.G., Yoneyama, K., Nogué, F., and Rameau, C. (211). Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138: Reprinted by permission from Macmillan Publishers Ltd: Parniske, M. (28) Arbuscular mycorrhiza: the mother of plant root endosymbiosis. Nat. Rev. Microbiol. 6: copyright 28. Strigolactones are present in nonvascular plants and some green algae G r e e n a l g a e Bryophytes mosses, liverworts Charales Chlorophyceae Lycopods club mosses Ferns Gymnosperms Plants Angiosperms s in whole plant responses - summary s have pleiotropic effects on plant development, mediated in part by auxin and other hormones Both partners benefit from the symbiosis The plant gets nitrogen and phosphorus from the soil by way of the symbiotic fungal association The fungus gets sugars produced by photosynthesis The arbuscule provides a large surface area for nutrient exchange Strigolactones regulate moss colony growth In wild-type moss, colony size decreases with increasing colony density In -deficient moss, colony size is insensitive to colony density s act like a quorumsensing molecule Strigolactones promote branching in arbuscular mycorrhizal fungi Time Zero Time 24 hours s promote hyphal branching levels are elevated in sorghum root exudates under low P and N control Low N Low P Low K Low Ca Low Mg deoxystrigol (pg/plant/5 days) Reproduced with permission from Proust, H., Hoffmann, B., Xie, X., Yoneyama, K., Schaefer, D.G., Yoneyama, K., Nogué, F., and Rameau, C. (211). Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138: Reprinted by permission from Macmillan Publishers Ltd: Akiyama, K., Matsuzaki, K.-i., and Hayashi, H. (25). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: copyright

8 The Plant Cell, ctober The nutrient-effect on production is plant-specific Strigolactones also promote Arabidopsis germination in some conditions nce attached to the host root, the plant grows and reproduces Seedling Flowering Tiny seeds Non leguminous, AM host plant (e.g sorghum) Leguminous plant Some non-am host plant Mustard Low P Low N r r Striga seeds show stronger seed dormancy and enhanced germination dependency on s Germination response can be studied in Arabidopsis Striga Instead, in low N, leguminous plants enter a symbiosis with nitrogen-fixing bacteria Tsuchiya, Y., Vidaurre, D., Toh, S., Hanada, A., Nambara, E., Kamiya, Y., Yamaguchi, S. and McCourt, P. (21). A smallmolecule screen identifies new functions for the plant hormone strigolactone. Nat.Chem. Biol. 6: Tobacco Dörr, I. (1997). How Striga parasitizes its host: a TEM and SEM study. Annals of Botany. 79: , by permission of xford University Press; USDA APHIS PPQ Archive; USDA APHIS PPQ Archive In nutrient-poor soils: synthesis increases Shoot branching decreases and root branching increases AM symbiosis increases These responses enhance plant survival under low nutrient conditions Striga species (witchweeds) are serious agricultural pests How can we move towards Strigaresistant crops? +P P Witchweed infestation Heavy Moderate Light Major cereal crops are infested: corn, sorghum, millet and rice 7 million hectares are infested Food productions for 3 million people are affected Financial loss is estimated to be approximately 1 billion USD No effective control measure has been developed Agricultural practices: Field treatments Allelopathic approaches Genetic approaches: Modify structure: encrypt the signal Suppress branching in deficient plants Striga hermonthica Striga asiatica Adapted from Ejeta, G. and Gressel, J. (eds) (27) Integrating new technologies for striga control: towards ending the witch-hunt. World Scientific Publishing, Singapore; Image sources: USDA APHIS PPQ Archive, Florida Division of Plant Industry Archive, Dept Agriculture and Consumer Services. Image courtesy of International Institute of Tropical Agriculture (IITA) H Strigolactones promote germination in parasitic and other plants Parasitism has evolved recently and several times Some plants are facultative parasites; others, like Striga, obligate parasites. Striga roots cannot grow normally. The primary root tip forms a haustorium specialized to penetrate host plant roots. robanche (broomrape)-infested carrot field Strigolactones were first characterized as inducers of Striga germination (196s) Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (28). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: Dörr, I. (1997). How Striga parasitizes its host: a TEM and SEM study. Annals of Botany. 79: , by permission of xford University Press; Reprinted from Westwood, J.H., Yoder, J.I., Timko, M.P., and depamphilis, C.W. (21) The evolution of parasitism in plants. Trends Plant Sci. 15: with permission from Elsevier. Photo credit Shmuel Golan courtesy of Yaakov Goldwasser 8

9 The Plant Cell, ctober H H Rice field infested with Striga Intercropping with beneficial plants can reduce Striga infestation Desmodium is a nitrogen-fixing legume that enriches the soil, and also produces allelopathic chemicals that interfere with Striga parasitism but an isomer of saturated GR24 promotes interactions with GR24 Saturated GR24 AM fungi Striga Striga asiatica Maize intercropped with Desmodium uncinatum Desmodium uncinatum Can we make synthetic s with beneficial but not detrimental effects? YES Can we engineer plants to make these? MAYBE Image courtesy of Prof. Julie Scholes & Mamadou Cissoko Hassanali, A., Herren, H., Khan, Z.R., Pickett, J.A. and Woodcock, C.M. (28). Integrated pest management: the push pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Phil. Trans. R. Soc. B 363: copyright 28 The Royal Society. Adapted from Akiyama, K., gasawara, H., Ito, S. and Hayashi, H. (21) Structural requirements of strigolactones for hyphal branching in. Plant Cell Physiol., 51: see also Boyer, F.D., de Saint Germain, A., Pillot, J.P., Pouvreau, J.B., Chen, V.X., Ramos, S., Stevenin, A., Simier, P., Delavault, P., Beau, J.M. and Rameau, C. (212). Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: molecule design for shoot branching. Plant Physiol. 159: Do all s promote Striga germination and affect branching? Can we engineer Striga resistance? Rice d1 -deficient mutant... A B C D 5-Deoxystrigol robanchol 2 -epi-orobanchol Sorgomol Solanacol robachyl acetate There are many different naturally occurring s how does their structure affect their function? (3) Shoot branching (2) Symbiosis (1) No germination of Striga seeds around the root (2) Reduced symbiosis (but not fully inhibited) (3) Too many shoot branches Are these effects separable? Parasitic plants infect 6% of farmlands in sub-saharan Africa robanchyl acetate 7-oxoorobanchyl acetate Fabacyl acetate Root parasite (1) Parasitism Sorgolactone Strigol Strigyl acetate Image source USDA APHIS PPQ Archive Agricultural practices can reduce crop losses from Striga Saturated (3,6'-dihydro-) GR24 isomers do not induce Striga germination Can we engineer Striga resistance? Rice d1 -deficient mutant... Before planting, apply germination stimulants to promote suicidal germination (no host = no survival) Apply fertilizers to reduce production by crop plants. These methods are prohibitively expensive in many parts of the developing world. Isomers of saturated GR24 Isomer I Isomer II Isomer III Isomer IV Enol ether GR24 (3) Shoot branching (2) Symbiosis (1) Parasitism Root parasite (1) No germination of Striga seeds around the root (2) Reduced symbiosis (but not fully inhibited) (3) Too many shoot branches Can we normalize shoot branching in -deficient mutants? Modify downstream component (e.g. d1 suppressor mutants) These experiments are in progress with a goal to producing Strigaresistant plants Photo courtesy Ken Hammond (USDA) 9

10 H H The Plant Cell, ctober Summary (1) Perception and signaling Conclusions and future directions Knowledge of the production and effects of s gives us the power to work towards eliminating the devastation of parasitic Striga Striga has a disproportionately large impact on those least equipped to control it, as it thrives in low-fertility soil - International Maize and Wheat Improvement Center (CIMMYT) de Saint Germain, A., Bonhomme, S., Boyer, F.D., and Rameau, C. (213). Novel insights into strigolactone distribution and signalling. Curr pin Plant Biol. 16: Photo courtesy CIMMYT Conclusions and future directions Strigolactones are synthesized in roots of nutrient-limited plants s enhance symbiosis s repress shoot branching and adventitious root formation s stimulate primary root growth, root hair elongation, secondary growth, and leaf senescence Conclusions and future directions How do s integrate with other hormones and signals to control shoot, root branching and leaf senescence? Can we modify the biosynthesis pathway to alter the types and activities of s produced? What are the evolutionary origins and ancestral functions of s? 1