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Fay<Wei!Li! Department!Of!Biology! Duke!Unive ! ! Seeing!the!Light:!the!Origin!and!Evolution!of!Plant!Photoreceptors! by! Fay<Wei!Li! Department!of!Biology! Duke!University! ! Date:_______________________! Approved:! ! ___________________________! Kathleen!M.!Pryer,!Supervisor! ! ___________________________! Meng!Chen! ! ___________________________! Sönke!Johnsen! ! ___________________________! Corbin!Jones! ! ___________________________! Sarah!Mathews! ! Dissertation!submitted!in!partial!fulfillment!of! the!requirements!for!the!degree!of!Doctor!of!Philosophy!in!the!Department!of! Biology!in!the!Graduate!School! of!Duke!University! ! 2015! ! ! i v! ! ! ABSTRACT! Seeing!the!Light:!the!Origin!and!Evolution!of!Plant!Photoreceptors! by! Fay<Wei!Li! Department!of!Biology! Duke!University! ! Date:_______________________! Approved:! ! ___________________________! Kathleen!M.!Pryer,!Supervisor! ! ___________________________! Meng!Chen! ! ___________________________! Sönke!Johnsen! ! ___________________________! Corbin!Jones! ! ___________________________! Sarah!Mathews! ! An!abstract!of!a!dissertation!submitted!in!partial!fulfillment!of! the!requirements!for!the!degree!of!Doctor!of!Philosophy!in!the!Department!of! Biology!in!the!Graduate!School! of!Duke!University! ! 2015! i v! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! Copyright!by! Fay<Wei!Li! 2015! ! ! ! Abstract Plants!use!an!array!of!photoreceptors!to!measure!the!quality,!quantity,!and!direction!of! light!in!order!to!respond!to!ever<changing!light!environments.!Photoreceptors!not!only!determine! how!and!when!individual!plants!complete!their!life!cycles,!but!they!also!have!a!profound!and! long<term!macroevolutionary!influence!on!species!diversification.!Despite!their!significances,! very!little!is!known!about!photoreceptors!across!plants!as!whole,!and!we!lack!a!comprehensive! view!of!photoreceptor!evolution.!! In!my!dissertation,!I!investigate!the!origin!and!evolution!of!three!of!the!most!prominent! photoreceptor!gene!families!in!plants:!phytochromes,!phototropins!and!neochromes.!Using! newly!available!transcriptomic!and!genomic!data,!I!completed!the!first!in<depth!survey!of!these! photoreceptor!families!across!land!plants,!green!algae,!red!algae,!glaucophytes,!cryptophytes,! haptophytes,!and!stramenopiles.!! Phytochromes!are!red/far<red!photoreceptors!that!play!essential!roles!in!seed! germination,!seedling!photomorphogenesis,!shade<avoidance,!dormancy,!circadian!rhythm,! phototropism,!and!flowering.!Here,!I!show!that!the!canonical!plant!phytochromes!originated!in!a! common!ancestor!of!streptophytes!(charophyte!green!algae!plus!land!plants),!and!I!identify!the! most!likely!sequence!whereby!the!plant!phytochrome!structure!evolved!from!its!ancestral! phytochrome.!Phytochromes!in!charophyte!algae!are!structurally!diverse,!including!canonical! and!non<canonical!forms,!whereas!in!land!plants,!phytochrome!structure!is!highly!conserved.! Liverworts,!hornworts,!and!Selaginella!apparently!possess!a!single!phytochrome!gene!copy,! whereas!independent!gene!duplications!occurred!within!mosses,!lycopods,!ferns,!and!seed! plants,!leading!to!diverse!phytochrome!families!in!these!clades.!My!detailed!phylogeny! ! iv! ! encompasses!all!of!green!plants!and!enables!me!to!not!only!uncover!new!phytochrome!lineages,! but!also!to!make!links!to!our!current!understanding!of!phytochrome!function!in!Arabidopsis!and! Physcomitrella5(the!major!model!organism!outside!of!flowering!plants).!Based!on!this!robust! evolutionary!framework,!I!propose!new!hypotheses!and!discuss!future!directions!to!study! phytochrome!mechanisms.! ! Phototropins!are!blue<light!photoreceptors!that!regulate!key!adaptive!physiological! responses,!including!shoot<positive!phototropism,!root<negative!phototropism,!chloroplast! accumulation/avoidance,!stomatal!opening,!circadian!rhythm,!leaf!expansion,!and!seedling! elongation!I!show!that!phototropins!originated!in!the!common!ancestor!of!Viridiplantae!(all! green!algae![charophytes,!chlorophytes,!prasinophytes]!plus!land!plants).!Phototropins! repeatedly!underwent!independent!duplications!in!all!major!plant!lineages!(mosses,!lycopods,! ferns!and!seed!plants),!except!for!liverworts!and!hornworts,!where!phototropin!is!a!single<copy! gene.!Following!each!major!duplication!event,!phototropins!subsequently!differentiated!in! parallel,!resulting!in!two!specialized!(yet!partially!overlapping)!functional!forms!that!primarily! mediate!either!low<!or!high<light!responses.!My!gene!phylogeny!further!suggests!that! phototropins!have!co<evolved!with!phytochromes,!as!is!evident!from!their!molecular!interactions! and!strikingly!similar!gene!duplication!patterns.!I!hypothesize!that!the!co<evolution!of! phototropins!with!phytochromes,!together!with!their!subsequent!convergent!functional! divergences!in!phototropic!responses,!contributed!to!the!success!of!plants!in!adapting!to!diverse! and!heterogeneous!habitats.! Neochromes!are!chimeric!photoreceptors!that,!by!fusing!phytochrome!and!phototropin! modules!into!a!single!protein,!are!able!to!use!both!red/far<red!and!blue!light!to!modulate! ! v! ! phototropic!responses.!Neochromes!were!first!discovered!in!ferns,!and!the!evolution!of! neochromes!was!implicated!as!a!key!innovation!that!facilitated!fern!diversification!under!the! low<light!angiosperm!canopies.!Despite!its!significance!from!an!evolutionary!standpoint,!the! origin!of!neochromes!has!remained!a!mystery.!Here!I!present!the!first!evidence!for!neochrome!in! hornworts!(a!bryophyte!lineage)!and!demonstrate!that!ferns!acquired!neochrome!from!hornworts! via!horizontal!gene!transfer!(HGT).!Fern!neochromes!are!nested!within!hornwort!neochromes!in! my!large<scale!phylogenetic!reconstructions!of!phototropin!and!phytochrome!gene!families.! Divergence!date!estimates!further!support!the!HGT!hypothesis,!with!fern!and!hornwort! neochromes!diverging!179!MYA,!long!after!the!split!between!the!two!plant!lineages!(at!least!400! MYA).!By!analyzing!the!draft!genome!of!the!Anthoceros!punctatus!hornwort,!I!also!discovered!a! novel!phototropin!gene!that!likely!represents!the!ancestral!lineage!of!the!neochrome!phototropin! module.!Thus,!a!neochrome!originating!in!hornworts!was!horizontally!transferred!to!ferns,!where! it!may!have!played!a!significant!role!in!the!diversification!of!modern!ferns.!! ! In!summary,!my!studies!identified!the!molecular!origins!of!phytochromes,!phototropins! and!neochromes,!and!reconstructed!their!respective!evolutionary!histories.!This!new!framework! for!photoreceptor!evolution!will!stimulate!new!research!linking!ecology,!evolution,!and! photochemistry!to!understand!how!plants!adapt!to!variable!light!environments.! ! vi! ! To!my!parents!who!showed!me!the!wonder!of!ferns…! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! vii! ! Contents Abstract!.........................................................................................................................................................!iv! List!of!Tables!.................................................................................................................................................!xi! List!of!Figures!..............................................................................................................................................!xii! Acknowledgements!...................................................................................................................................!xiv! Introduction!....................................................................................................................................................1! 1.!The!origin!and!evolution!of!phytochromes!...........................................................................................3! 1.1!Introduction!.......................................................................................................................................3! 1.2!Results!................................................................................................................................................5! 1.2.1!Names!for!phytochrome!gene!lineages!...................................................................................7! 1.2.2!Stramenopiles!and!haptophytes!...............................................................................................7! 1.2.3!Red!algae!......................................................................................................................................9! 1.2.4!Glaucophytes!...............................................................................................................................9! 1.2.5!Cryptophytes!.............................................................................................................................10! 1.2.6!Viridiplantae!..............................................................................................................................11! 1.2.7!Neochromes!...............................................................................................................................13! 1.2.8!Bryophytes!.................................................................................................................................14! 1.2.9!Lycophytes!.................................................................................................................................15! 1.2.10!Ferns!..........................................................................................................................................17! 1.2.11!Seed!plants!...............................................................................................................................18!
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  • Distribution and Phylogenetic Significance of the 71-Kb Inversion
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