Koppisiemeniset eli kukkakasvit. Koppisiemeniset: Yleiset piirteet Kasvisystematiikka: maakasvit. Sukupolvenvuorottelu. Koppisiemenisten ekspansio

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1 eli kukkakasvit Yleiskuva : Yleiset piirteet Kasvisystematiikka: maakasvit Jari Oksanen Biologian tutkinto-ohjelma 2016 Viridiplantae muut viherlevät sisarlevät sammalet jne maakasvit lieot putkilokasvit sanikkaiset+kortteet monilofyytit paljassiemeniset siemenkasvit koppisiemeniset Nykyään > 400 heimoa ja ainakin lajia sanikkaisia > , paljassiemenisiä n. 750 Ensimmäiset fossilit liitukaudelta n. 140 milj. v sitten Kasvien valtaryhmä tertiaarikaudelta n. 65 milj. v sitten (K/T-raja) Tunnuspiirteinä kukka, jossa voimakkaasti redusoituneet gametofyytit Tehokas johtosolukko ja sopeutumia kuivuuteen Jari Oksanen (Biologia) : Yleiset piirteet / 40 Jari Oksanen (Biologia) : Yleiset piirteet / 40 Koppisiemenisten ekspansio Yleiskuva Sukupolvenvuorottelu Yleiskuva Jari Oksanen (Biologia) : Yleiset piirteet / 40 Tärkeimmät erot paljassiemenisiin: Suljettu alkiorakko ( -gametofyytti) Kaksi siemenaiheen kalvoa (integumenttia) Siitepölyhiukkanen ja siiteputki -gametofyytti kehittyy siitepölyhiukkasessa Kaksoishedelmöitys endospermi Kukkalehdet Putkilot Jari Oksanen (Biologia) : Yleiset piirteet / 40

2 Luokittelun pääpiirteet Luokittelun pääpiirteet Neljä pääryhmää Luokittelun pääpiirteet 1 ANA eli ANITA: erillisiä ryhmiä, jotka kaikkien muiden siskoja Amborellaceae, Nymphaeaceae, Austrobaileyales Primitiivisiä piirteitä: Amborellalla ei putkiloita Emilehti putkimainen, laaja luottipinta 2 Magnolidit Pidettiin ennen koppisiemenisten kantaryhmänä Lukuisia primitiivisiä piirteitä, mm. lukuisia, heikosti erilaistuneita kukkalehtiä 3 Yksisirkkaiset (Monocots) Yksi sirkkalehti Silposuoniset lehdet 4 Kaksisirkkaiset (Dicots) Kolmiaukkoinen (trikolpaattinen) siitepöly Ponsi ja palho selvästi erilaistuneet Yksi- ja kaksisirkkaiset suurin ja laaja-alaisin ryhmä Jari Oksanen (Biologia) : Yleiset piirteet / 40 Jari Oksanen (Biologia) : Yleiset piirteet / 40 Yksisirkkaiset ja kaksisirkkaiset Luokittelun pääpiirteet Angiosperm Phylogeny Group IV Luokittelun pääpiirteet Magnoliids Commelinids Fabids Amborellales Nymphaeales Austrobaileyales Magnoliales Laurales Piperales Canellales Chloranthales Arecales Poales Commelinales Zing iberales Asparagales Liliales Dioscoreales Pandanales Petros aviales Alismatales Acorales Ceratophyllales Ranunculales Proteales Trochodendrales Buxales Gunnerales Fabales Rosales Fagales Cucurbitales Oxalidales Malpighiales Celastrales Zygophyllales Geraniales Myrtales Crossosomatales Picramniales Malvales Brassicales Huerteales Sapindales Vitales Saxifragales Dilleniales Berberidopsidales Santalales Caryophyllales Cornales Ericales Aquifoliales Asterales Escalloniales Bruniales Apiales Dipsacales Paracryphiales Solanales Lamiales Vahliales Gentianales Boraginales Garryales Mettenius ales Icacinales Monocots Rosids Malvids Campanulids. APG IV 3 Superrosids Asterids Superasterids Lamiids Researchers have speculated about what analyses of low-copy nuclear genes would reveal about plant relationships and whether these relationships would Jari Oksanen (Biologia) : Yleiset piirteet / 40 Angiosperms Eudicots Jari Oksanen (Biologia) : Yleiset piirteet / 40 e s. e of Soltis et al. (2011), l et al. (2015). Soltis om all three genomes

3 angiosperm transcript assemblies, into this gene tinued. Indeed, many gene lineages with genes (VND7 and NAC083) alsofirstappeared atthis classification, and manually reevaluated the origin inferred Evoluution to have päälinjat specific stamen (39), carpel (39), time, even though Amborella does not produce Evoluution päälinjat of orthogroups around the MRCAs of seed plants and ovule (40) functionsapparentlyarose after vessels, but only tracheids (see below). Perhaps and angiosperms, thereby resolving or refining the the origin of angiosperms, within evolutionarily surprisingly, the most highly enriched Amborella: GO terms trichopoda, in kaikkien an understory shrub kukkien endemic to sisar New Caledonia, is the sole surviving sister species origin of 5210 orthogroups, 1179 (23%) of which derived angiosperm lineages (table S18). orthogroups derived in angiosperms of all were other associated with homeostatic processes for (GO: ; inferring features of the first flowering plants and identifies an ancient angiosperm-wide whole-genome living flowering plants (angiosperms). The Amborella genome provides an exceptional reference are specific to angiosperms or have diverged sufficiently such that none of the gymnosperm homo- explained by novel gene lineages that first appeared 18.9-fold enrichment). Relevant Whereas the origin of the flower may be partly Kehittyivät paljassiemenisistä tai suoraan siemensaniaisista duplication to the importance of plant-herbivore coevolution laminar thestamens. diver- (red star). Amborella flowers have spirally arranged tepals, unfused carpels (female; shown), and logs were detected, with 4031 (77%) present in with the origin of the angiosperms, other floral genes, Amborella Genome Project, Science 342 (2013). DOI: /science the MRCA Bennettitales of seed plants (valekäpypalmut): (table S13). including myösputative kukkia B-class mutta (that is, lienee petal- and stamenspecific) sification of angiosperms and insects (43, 44), the gene targets (41), predate the origin of an- next most highly enriched GO classification was The large number of orthogroups first appearing in angiosperms suggests that a diverse collecgiosperms. More than 70% of the gene lineages for genes involved in response to external stimuli käpypalmujen sisar tion ofsäteettäissymmetriset novel gene functions was likely associated siemenet with known roles in flowering, including genes involved (GO: ; 10.9-fold enrichment), including in floral timing and initiation (CO, SOC1, those with expression elicited by herbivory. with the origin of flowering plants. Analyses of Lehdet GO annotations megafyllejä, for genes in angiosperm-derived jotka kehittyivät VIN3, verkkosuonisiksi VEL1), meristem identity (ULT1, kasvulehdiksi TFL2), and ja Enrichment patterns for functional categories kukkalehdiksi orthogroups revealed the origin of orthogroups floral structure (AFO, AP2, ETT, HUA2, HEN4, were similar in the ancestral seed plant and ancestral angiosperm (table S16), including novel with functions associated with key innovations KAN, RPL, JAG), were present in the MRCA of Kasvullisten defining the flowering osien plant clade rakenne (table S16) kehittyi (17). alltuulenkestäväksi extant seed plants (table S16) (17). Orthogroups lineages of genes involved in reproductive, regulatory, and developmental processes. GO classi- GO annotations related to reproduction (flower for other major components of the floral regulatory development, Vähemmän reproductive tukisolukkoa developmental process, pathway are older still, with core components of the fications associated with pollen-pistil interaction pollination, Liuskaiset and similar lehdet, terms), including joustava MADSbox lehtiruoti pathway present in the ancestral vascular plant and epigenetic modification were enriched in or- gene lineages (see below), were overrepre- (for example, LFY, phytochromes, CLV, SKP1, GA1, thogroups arising on the branch leading to seed Myös sented inkukkalehdet this set of orthogroups. lehtijohdannaisia: Genes with roles SEU, HEN1, hyvinandfve). monimuotoisia ja plants, but not in the lineage leading to the ancestral angiosperm (table S16), the former per- in Arabidopsis floral development (table S17) are Together, these observations suggest that kehittyneitä rakenteita included in 201 orthogroups, 18 of which were orthologs of most floral genes existed long before haps indicating that some angiosperm-specific evolutionarily derived in the MRCA of angiosperms. their specific roles were established in flowering, reproductive features predated angiospermous (enclosed ovule) reproduction. *All authors and their affiliations and contributions are listed at the end of the paper. Putkilot (trakeat): paljassiemenisten putkisoluista (trakeidit) Significant enrichments were also observed for and that they were later co-opted to serve floral functions. After the origin of angiosperms, new genes kehittyneitä several classes of regulatory tehokkaita genes (transcription, vedenjohtimia Amborellan genomi sekvensoitu: voidaan arvioida, mitä on tapahtunut Corresponding author. cwd3@psu.edu. Contact information for working groups is provided in the authorship details. regulation of gene expression and of cellular, biochemical, johtamiseen and metabolic processes) ja as rungon well as genes tukemiseen rowly parse functions erilaiset associated solutyypit with flower devel- Expansions of many gene families are evident in originated or were recruited to refine or more nar- Gene Family Expansions in Angiosperms koppisiemenisten evoluutiossa ennen ja jälkeen Amborella-haaran Veden involved in various developmental processes. opment. This pattern is consistent with the observation Amborella,andphylogeneticanalysesindicatethat SCIENCE VOL DECEMBER 2013 ( hardwood ) These include genes involved in carpel development that the floral organ transcriptional program is cana- such expansions occurred in the ancestral angio- Published by AAAS (CRABS CLAW), endosperm development lized (entrained) in eudicots relative to the less organsperm, accompanying innovations associated with Jari(AGL62), Oksanen (Biologia) stem cell maintenance in: meristems constrained Yleiset piirteet transcriptomes of earlier-diverging, 2016 less angiosperm 12 / 40 origin. Using Amborella asjari a reference, Oksanen (Biologia) : Yleiset piirteet / 40 (WUSCHEL), and flowering time (FRIGIDA), species-diverse angiosperm lineages (42). we examined patterns of gene family diversification suggesting that they might be key components Many of the novel gene lineages that first in angiosperm evolution, often in association with underlying the origin of the flower. arose Evoluution in angiosperms päälinjat play no specific role in phenotypic divergence among angiosperm lineages. Evoluution päälinjat Once a functional flower evolved, genetic innovations related to reproductive biology con- genes with specific functions in vessel formation reproductive processes. Orthogroups containing MADS-Box Genes ja evoluutio Koppisiemenisten rakenteiden evoluution päälinjat Uudet ja hävinneet geeniryhmät Fig. 3. Ancestral reconstruction of gene family content in land plants. Orthogroup gains and losses are inferred from the global gene family classification of proteins from sequenced plant genomes using a Wagner parsimony framework (17). Triangles are proportional to the number of orthogroup gains (green) and losses (orange). Actual values for the gains and losses in this analysis are provided in table S14; an analogous likelihoodbased analysis is provided in table S gains/losses Physcomitrella patens Selaginella moellendorffii Amborella trichopoda Phoenix dactylifera Musa acuminata Oryza sativa Brachypodium distachyon Sorghum bicolor vinifera Glycine max Medicago truncatula Fragaria vesca Populus trichocarpa Theobroma cacao Carica papaya Thellungiella parvula Arabidopsis thaliana Solanum lycopersicum Solanum tuberosum Jari Oksanen (Biologia) : Yleiset piirteet / 40 MADS-box transcription factors are among the most important regulators of flower development. The Amborella genome encodes 36 MADS-box genes (table S19) (17), fewer than in other angiosperms (for example, Arabidopsis and rice), but consistent with the lack of a lineage-specific WGD. These genes belong to 21 clades, each of which includes genes from at least one other major lineage of angiosperms, implying that a minimum set of 21 MADS-box genes existed in the MRCA of extant angiosperms (figs. S19 and S20). The Amborella genome reveals that floral organ identity genes from eight major lineages (that is, AP1/SQUA, AP3/DEF, PI/GLO, AG, STK, AGL2/SEP1, AGL9/SEP3,and AGL6;Fig.4A)existedintheMRCAofextantangiosperms and were likely derived from three ancestral lineages in the MRCA of extant seed plants. These data support the hypothesis that duplication and diversification of floral MADS-box genes likely occurred before the origin of extant angiosperms, despite being tightly associated with the origin of the flower. Furthermore, the previously presumed monocot-specific OsMADS32 and eudicot-specific TM8 gene lineages (fig. S20) (45 47) have orthologs in Amborella,suggesting thatthey were likely present in the earliest angiosperms and were subsequently Amborella Genome Project, Science 342 (2013). lost in eudicots or monocots, respectively. Koppisiemenisten yhteinen esiäiti: kukka, kukkalehdet, siemenen kehitys, endospermi, kukan kehityksen ajoitus Myöhemmin kehittyivät heteiden ja emien kehityksen vaihteleva säätely eri linjoissa Osa hedelmöitykseen (emi, hede) liittyvistä geeneistä kehittynyt ennen koppisiemenisten eroa paljassiemenisistä Putkiloiden kehitys (vaikka Amborellalla ei ole putkilosoluja) Kemiallinen puolustautuminen herbivoreilta Kukkien tuoksun aiheuttavat sekundaarikemia kehittyi sen jälkeen, kun Amborella erosi muista koppisiemenisistä Jari Oksanen (Biologia) : Yleiset piirteet / 40 via mitochon Amborella. S DOI: S. Chamala, A genome of th Amborella. S DOI:

4 3) (17) andthuscorregenome equivalents of NA. Most (86%) of the onsistent with the high mtdna in angiosperms the 753 kb shares 90% one or more sequenced l genomes (fig. S4). This lihood evilla mtdna. enetreesof lgae reveal ella mtdna. e fig. S8 for lues 50% after each corresponds n kb (figs. S2 pond to 0.1 to (H)] subranches are. (E to H) ngiosperms for HGT to order: light (F)]; brown, agales (H). lastid, gene b IGT; gene T; red Amb, ia HGT. Outsee fig. S19 yses, includtes the rps7- fig. S19). Analysis of the remaining 10 kb of origin (Fig. 1) (13), some of its foreign DNA may ptdna, which probably entered Amborella from be the product of serial, angiosperm-to-angiospermto-angiosperm HGT (13). In particular, the rbcl Evoluution päälinjat foreign mitochondria, identified donors with much greater specificity than did the mitochondrial gene gene of santalalean origin (Fig. 2E) resides only analyses (13). Four of the HGT plastid regions 3 kb from the Bambusa-derived sequence on the identified Fagales, Oxalidales, or the predominantly same 27-kb foreign tract (Fig. 1B). Because all parasitic Santalales as the donor, while a four genes of meaningful length on this tract fifth pointed to Magnoliidae (Fig. 2, E to H, and evidently came from core eudicots (fig. S14), and Amborella: Mitokondrioissa horisontaalisia geenisiirtymiä Putkilokasveista (Santalales: loisia), sammalista, viherlevistä (jäkälät) 66 A atp Arabidopsis 91 Nicotiana 88 Beta Amb Amb 1276 Cycas Pleurozia 54 Marchantia 52 Nothoceros Amb 1657 Physcomitrella Chara Chaetosphaeridium Chlorokybus Ostreococcus Nephroselmis Oltmannsiellopsis Amb C 1408 Amb B 1505 Coccomyxa Amb A 403 Helicosporidium Prototheca Amb 3070 Carica Oryza B atp Amb 617 Nicotiana Arabidopsis Carica Beta Amb 2196 Oryza 82 Amb 2809 Amb Pleurozia Nothoceros Amb 488 Cycas 57 Marchantia Amb 269 Physcomitrella Chara Chaetosphaeridium 86 Micromonas Ostreococcus Chlorokybus Oltmannsiellopsis Nephroselmis Amb D 2333 Amb C 3 Amb B 336 Coccomyxa Amb A 394 Helicosporidium Prototheca 64 C atp Arabidopsis Carica Oryza Beta Amb 3487 Amb 917 Amb 2226 Nicotiana Cycas Amb Amb Pleurozia Marchantia Amb 268 Physcomitrella Chara Chaetosphaeridium Helicosporidium Prototheca Oltmannsiellopsis Nephroselmis Amb D 2332 Amb C 5 Amb B 335 Amb A 395 Coccomyxa Ostreococcus Chlorokybus 97 E F Rice et al. 2013, Science G 342: H 80 Coffea 81 Coffea 79 Coffea 86 rbcl 52 Nicotiana psbcd 94 Nicotiana psaa 89 Nicotiana rps7 76 Helianthus Daucus 93 Daucus 99 Nicotiana Coffea Daucus Rhododendron Helianthus Helianthus Helianthus Jari Oksanen Berberidopsis (Biologia) 88 : Rhododendron Yleiset piirteet Rhododendron Berberidopsis / Harmandia Spinacia 76 Phoradendron Rhododendron 94 Hondurodendron Plumbago Ximenia Plumbago 67 Amb 3078 Berberidopsis Spinacia Spinacia 65 Phanerodiscus 99 Amb 3547 Plumbago 89 Phoradendron Phoradendron 97 Phoradendron Evoluution Berberidopsis päälinjat 82 Ximenia 59 Comandra Ximenia 76 Amb Oxalis Engomegoma Oxalis Oxalis 77 Populus Ximenia Populus Euonymus 81 Euonymus Plumbago 70 Euonymus 51 Populus 97 Amb Oxalis Cucumis 65 Cucumis 61 Quercus Euonymus 64 Quercus 76 Quercus Cucumis Quercus Arabidopsis Arabidopsis 93 Arabidopsis Arabidopsis 58 Gossypium Trochodendron Gossypium 85 Trochodendron Gossypium 74 Platanus Gossypium Joillain alkeellisina pidetyillä ryhmillä emi lehtimäinen: kourumainen, 69 Buxus Platanus Buxus Buxus Trochodendron Buxus Platanus 82 sauma laaja luottipinta Trochodendron Platanus Typha Drimys 68 Typha Ceratophyllum 78 Yucca Chloranthus 70 Yucca 90 Lemna Yucca Acorus Drimys Acorus Lemna Lemna Nykyään nähdään usein johdettuna ominaisuutena Typha 74 Acorus 72 Yucca Chloranthus 96 Ceratophyllum 95 Drimys 70 Acorus Lemna 53 Ceratophyllum Magnoliideilla usein heteen palhot lehtimäisiä ja58vaihettuvat Drimys 77 Chloranthus 74 Nuphar Nymphaea Illicium 81 Nymphaea Illicium Ceratophyllum Nymphaea Illicium Chloranthus terälehdiksi (joutoheteet): ehkä johdettu ominaisuus Amb IGT Amb IGT Amb plastid Nuphar Nuphar Amb plastid Amb IGT Amb IGT Nymphaea Illicium Amb plastid Amb plastid Nuphar Emiö ja hetiö 20 DECEMBER 2013 VOL 342 SCIENCE Drimys piperita (Canellales: Winteraceae) D cob Marchantia Amb 16 Physcomitrella Chara Chaetosphaeridium Chlorokybus Ostreococcus Micromonas Nephroselmis Amb C 2284 Amb B 346 Coccomyxa Amb A 385 Helicosporidium Prototheca Oltmannsiellopsis 53 Oryza Arabidopsis 95 Nicotiana Beta Carica Amb 506 Amb 2013 Cycas Nothoceros Pleurozia Degeneria sp. (Magnoliales: Degeneriaceae) Jari Oksanen (Biologia) : Yleiset piirteet / 40 Kukan synty Lyhytnivelvälinen heterosporangiaattinen strobilus Päätteinen: pituuskasvu ei jatku kukasta Megasprofofylli = emi ( ) mikrosporofylli = hede ( ) Kukkalehdet ulkoa keskelle: 1 Verholehdet (verhiö, calyx) 2 Terälehdet (teriö, corolla) 3 Hedelehdet (hetiö, androecium) 4 Emilehdet (emiö, gynoecium) Primitiivisessä kukassa kukkalehdet kierteisesti ja raja tyyppien välillä voi olla liukuva Evoluution päälinjat Jari Oksanen (Biologia) : Yleiset piirteet / 40 Ensimmäiset kukkafossiilit Archaeanthus Fossiilit Fossiileja kukkien osista, hedelmistä, lehdistä, puuaineksesta ja siitepölyhiukkasista Kaksi varhaista kukkatyyppiä: 1 Pienet (mahdollisesti yksineuvoiset) kukat, vähän kukkalehtiä: kuten Chloranthales ja Piperales 2 Suuret kaksineuvoiset kukat (> 6.5 cm), lukuisia kukkalehtiä, joskus heikosti erilaistuneet: kuten Magnoliales Magnoliales: pidettiin ennen primitiivisenä, mutta sopeumia kovakuoriaispölytykseen kovakuoriaispölytykseen: korkea kukkapohjus, lehtimäistä hedettä, iso yksittäinen kukka Primitiivinen kukka: 2kehäkiehkuraa, 2 hedekiehkuraa, putkimaiset emiöt, terttumainen kukinto Jari Oksanen (Biologia) : Yleiset piirteet / 40

5 Siemenet ja siitepölyhiukkaset Fossiilit Lehtifossiilit Fossiilit Varhaisimmat hedelmät ja siemenet n. 121 milj. v vanhoja Ceratophyllales, Ranunculales... Siemenet pieniä, 1 40 mm: r-strategisteja? Siitepölyhiukkaset n. 130 milj. v vanhoja, runsaasti fossiileja Läpimitta µm Neljä erilaista rakennetyyppiä iturakojen perusteella Clavatipollenites Chloranthales Liliacidites Liliales Tricolpites (myöhäinen) nykyiset kaksisirkkaiset Lehdet megafyllejä Ensimmäiset fossiilit n. 120 milj. v sitten Sulkamais-verkkomainen suonitus, joka muodostaa erillisiä pintoja, joihin myös päättyy suonia: kaksisirkkaiset Silposuonisia eli yhdensuuntainen suonitus ja poikittaiset suonet heikkoja: yksisirkkaiset Jari Oksanen (Biologia) : Yleiset piirteet / 40 Jari Oksanen (Biologia) : Yleiset piirteet / 40 Lehtityypit liitukaudella Fossiilit Varhaiset koppisiemeniset 1 Puita Kuten nykyinen Magnoliales ja Laurales Vallitseva hypoteesi takavuosina: Magnoliales-kukkaa pidettiin basaalisena, ja kaikki ryhmän nykylajit puita 2 Juurehtivia ruohoja Kuten nykyinen Piperales Nykyään suosittu, koska varhaisissa fossiileissa vähän puuaineista ja varhaiset lehdet ja siemenet pieniä Puumaisia fossiileja vasta tertiäärikaudella Sekä nykyiset yksisirkkaiset että (varsinaiset) kaksisirkkaiset (eudicots) kehittyneet varhaisemmista muodoista Yksisirkkaiset ruohovartisia: fossiiliaineisto huonommin säilynyt Jari Oksanen (Biologia) : Yleiset piirteet / 40 Jari Oksanen (Biologia) : Yleiset piirteet / 40

6 and Superasteridae (superasterids) (see ref. 10 for lineage definitions); to uncertainty about whether species in the freezing-unexposed state these clades represent Koppisiemenisten, 22%, 3%, synty 34% and 34%, respectively, of all actually lacked an ability to cope with freezing(supplementary Information). Across angiosperms, asymmetry of transition rates led to numer- extant angiosperm species. Synty ja radiaatio Acrosswoody angiosperms, a modelthatassumedcoordinated evolution of leaf phenology and climate occupancy was strongly supported freezing-exposed states (Fig. 3a and Extended Data Table Phytologist 3). The large ous extant species in the woody Ajoitettu freezing-unexposed puu and herbaceous New Research 271 over a model that assumed they evolved independently (Akaike information criteria (DAIC) ; Fig. 2a and Extended Data Table 2). ing to our model, was the result of this state being persistent Ordovician Sil. (Fig. Devonian 3a). Carnoniferous Permian Triassic Jurassic Cretaceous Paleogene Neo. number of extant species in the woody freezing-unexposed state, accord- RESEARCH LETTER Deciduous freezing-exposed and evergreen freezing-unexposed were Even within monocots, where relatively few woody species exist, the Malvid 82.8 Ma Arabidopsis thaliana 17 highly persistent character states (Fig. 2a, as indicated by size of the woody freezing-unexposedstatewas stronglypersistent. The herbaceous Fabid 124 Ma Populus trichocarpa onary solutions Ilmeisesti.0 uc across asyntyivät species range; paleotropiikissa and circles, freezing and Extended exposed, increases Data jaencountering levisivät Table as conduit 3); persistence diameter viileämpiin times increases (that is, expected 5. Three evolutionary freezing-exposed solutions state, on.0 theuc other across hand, a species had low range; persistence and times, freezing exposed, encountering Mesangiospermae Monocot ) woody species temperatures #0uC somewhere across time until a species state change) range. seemingly This are defined dichotomy arose as the to address inverse ofthe challenges sum ofestimated freezing: indicating (1) woody thatspecies the numerous temperatures extant species #0uC(Nsomewhere 5 4,066 outacross of 12,706 a species range. This dichotomy Sorghum bicolor Ma vyöhykkeisiin milj. v myöhemmin Chloranthaceae hydraulic funcf small-diameter common than the evolution of climate presence occupancy; of freezing, this assumes that climate tracking through transition environmental rates away withstood changes from a given freezing is more character temperatures state. Therefore, without serious in the loss species of hydraulic for whichfunc- tion the is data areassumes available) that wereclimate due to many tracking rapid through transitions environmental changes is more.7 Ma Chloranthus spicatus by more deciduous building likely safe state to water-transport was far more stable networks thanconsisting the bothof into small-diameter and out of this character common state than (Fig. the 3a). evolution Climate occupancy of climatewas occupancy; this is more likely to Magnoliid Ma tulipifera tion by becoms; and (3) herb- Angiospermae Ensimmäiset be true if freezing exposure (135 milj. has a physiological evergreen v) varmasti one. cost We conduits; in also ajoitetut regions found(2) that without woody leaf ja phenology tunnistetut species shut was generally down siitepölyt hydraulic about much function more bylabile becoming occupancy deciduous, (climate:trait dropping rate leaves ratioduring ), freezing and it periods; Furthermore, and (3) the herb- predominant freezing pathway than growth be trueform if freezing (climate:trait exposure ratehas ratio a physiological ). cost in regions without Austrobaileyales 124 Ma Illicium oligandrum 12 Lähi-idästä freezing 21.Specieswerefurtherdistinguishedbyleafphenology(deciduous labile climate ja Pohjois-Afrikasta, jotka tuolloin 25 N 21.Specieswerefurtherdistinguishedbyleafphenology(deciduous within angiosperms from was also far more likely Nymphaeales 124 Ma Nymphaea alba ply constructed or evergreen); conduit diameter (large $0.044 mm, oraceous to small,0.044 species evolve as mm; largely a response avoided to freezing a changeby insenescing environment rather than Amborella woody cheaplyfreezing-unexposed constructed or evergreen); state to theconduit herbaceous diameter freezing-exposed (large $0.044 mm, or small,0.044 mm; or underground Nopea as mm radiaatio diameter ismyös the diameter viileämmillä above whichaboveground arising before freezing-induced tissue encountering and overwintering, freezing (that probably is, cli-amate occupancy evolved Spermatophyta seeds state or was underground to first evolve the as herbaceous mm diameter habit andis subsequently the diameter enter above which freezing-induced leveysasteilla Amborella trichopoda Gnetales ms are likely to embolisms are believed to become frequent at modest storage first; tensions organs. Fig. 2c). 22 ); and However, the order in which angiosperms habitats with are likely freezing-exposed to embolisms conditions are believed (that is, tothe become trait evolved frequent at modest tensions 22 ); and Similarly, across woody Ma Welwitschia mirabilis 6 Coniferae Ma d persistence in Paljassiemeniset growth form (woody orsäilyivät herbaceous, with pitkään woodyvallitsevina have species acquired angiosperms, definedthesea as viileämmässä solutions model assuming relative coordinated to exposure to before and persistence the climate occupancy; in growth Fig. form 3b). This, (woody in combination or herbaceous, with with the woody species defined as Pinaceae evolution of conduit diameter size and climate occupancy was strongly conduit diameter results, suggests that lineages that successfully colonized new freezing environments were probably predisposed to do so, Ma Pinus thunbergii those maintaining a prominent aboveground stemthe that cold is persistent Euphyllophyta Cupressophyta 8 vuodenaikaisilmastossa 16 remains unclear. those maintaining a prominent aboveground stem that is persistent supported over a model that assumed they evolved independently Ma Cryptomeria jabonica and those with over time and with changing environmental (DAIC ; conditions; Fig. 2b Proportions andsee Extended of Data herbaceous Table 2). species, Both climate deciduous occupancy states with (freezing woody small growth exposed water-conducting habits and freezing as unexposed) conduits increase combina- towards the Although poles Ginkgo biloba species at least and for those these with two traits. over time and with changing environmental conditions; see Extended 5 Acrogymnospermae Ma 7 Ginkgo Ma oles 1,4,17,18, and Data Fig. 1 for examples of angiosperms Koppisiemenisillä adaptaatioita kuivuuteen: nahkeat, pienet lehdet, 1,4,17,18 our, focus and here Data is Fig. on evolutionary 1 for examples linksofbetween angiosperms specieswith woody growth habits as Cycad ted that herballel 19.However, kova habit bysiemenkuori, order within angiosperms). tehokas Data Table vedenkuljetus 3). Additionally, ceousness noand putkiloissa species ability with to cope largewith conduits freezing wereevolved in the inspecies parallel to 19.However, cope with freezing, habitwe bynote order that within differential angiosperms). diversification Fern we define them, and Extended Data tion Table with1 small for a conduits breakdown an earlier were oflimited highly growth persistent survey of(fig. angiosperm 2b and Extended families indicated distributions thatwith herba- respect we todefine freezing them, conditions and Extended and traits Data thattable allow1 for a breakdown of growth Cycas taitungensis Tracheophyta Ma Psilotum nudum 454 unctional evoluions of different between climate occupancy states were actersignificantly state (that is, associated tion short ofpersistence angiosperms with shiftstime). is uncertain. As withwe leafdissect phenology, the contributions determining of different why we see species between where climate we do occupancy today. Forstates instance, wereherbs significantly associated with shifts Among woody species we asked freezing-exposed whether evolutionary state, exactly indicating how transitions global-scale that this isecological a highly transitory patterns are char- linkedrates to functional 23 and vagility evolu- among lineages Amongalso woody certainly species played wetheir asked parts whether in evolutionary transitions Lycopsid Ma Stomatophytes 3 Selaginella moellendorfii Rikkaruohomaisen elinkierron ja lehtien kausivihannuuden synty 1042 Hornwort Ma Anthoceros formosae 2 periodic freezese traits (that is, asked whether evolutionary transitions between climate ingoccupancy and assessstates likely pathways by which clades acquired Additionally, these traits growth (that is, formasked may whether influenceevolutionary a plant s ability transitions to disperse between to climate occupancy states in leaf phenology and/or conduit diameter. climate occupancy Among all evolutionary and angiosperms conduit diameter solutions we were allowing similar angiosperms in their overall to copemay withave periodic higherfreez- speciation in leaf and/or phenology extinction and/or rates than conduit woody diameter. taxa 24. Among all angiosperms we 1042 lability (climate:trait rate ratio ); however, a shift into environments with freezing temperatures was far more likely to occur after Moss Ma Physocomitrella patens 1042 Liverwort ait evolution). were significantly associated with shifts in growth form. timing We determined of evolution in climate occupancy relative and to trait colonize evolution). newly emerging were significantly locations withassociated freezing temperatures with shifts in 25. growth form. We determined Embryophyta Marchantia polymorpha conduits had already shifted fromlarge tosmall (that is, the trait evolved iosperm growth the relative lability of climate occupancy before climate (exposure occupancy; to We freezing) compiled Fig. 2d). versus a very large species-level database oftestsofthesealternativesarecritical angiosperm growth the relative forfullyunderstanding lability of climate occupancy howangios-(exposurperms radiated into freezing environments, but such500analyses require to freezing) versus plant species 20 traits (growth form, leaf phenology or conduit diameter) habits by (49,064 summing species, which is 16.4% of accepted land plant species 20 traits (growth form, leaf phenology or conduit Time diameter) in millions of years by before summing present (Ma) Evolutionary shifts in growth habit were also strongly coordinated an even more complete record of global distributions of vagility and Fig. 2 A representative tree of relationships between model representatives of the major land plant lineages whose plastid or nuclear genomes nology, conduit Jari alloksanen climate (Biologia) occupancy transitionswith and : shifts dividing in climate. by Yleiset the in The However, sumpiirteet Plant of all List; thetrait nature of coordination varied 2016 leaf considerably summary among based major diameter on these angiosperm and evolutio- freezing clades climate (Extended exposure. Data Table To trace 3), asspecies sampled traitphylogeny. and climatethese transitions. 25 phenology, / 40 conduit all climate Jari occupancy Oksanen (Biologia) transitions and dividing have been fully sequenced. The topology: by the sum of based upon a consensus ofyleiset all trait growth habit across land plants and a comparably more completely the most well-supported piirteet relationships as reviewed in recent literature / 40 (Qiu, 2008; Forest & Chase, 2009; Magallón, 2009; Magallón & Hilu, 2009; Renner, 2009). Calibrations are presented for all 17 nodes, rait and climate transitions. We also devised a novel are non-trivial We also improvements devised a novel consisting ofasa hardwe summary minimum cur- generated havean growth unpar- habitnary data transition for only 16% rates of that accepted provides land the plants likeliest 20 pathways from the pur- based on these evolutio- constraint (bold) and a soft maximum constraint (not bold) for each. Justifications for these minima and maxima are provided in the text, and an overview in Table 1. The tree has been scaled to time on the basis of the minimum constraints. rated an unpard plant species ported early angiosperm (woody,. evergreen, monocots). with Of 104 large Koppisiemenisten alleled models conduits time-scaled evaluated, and syntymolecular a 40-parameter phylogeny model for allow- 32,223 (R.G.F. land plant et al., manuscript species ported submitted) earlyand angiosperm molecular(woody, and climate evergreen, data with large conduits Koppisiemenisten and synty nary transition rates that providesdid theoverall likeliest transition pathways occupancy rates from (superrosids the relationships pur-and superasterids over evolutionary. magnoliids time, werently minimum constraint is derived from fossils classified within this diverse pollen group (> 80 species; Pacltová, 11) larplants_tank freezing unexposed) to a plant ing witheach traits major forlineage freezing our have database conditions. its own (Fig. transition 1; matrix received most for 26% (12,706 species) of freezing those taxa. unexposed) Total traitto records Brassicales a plant are andfewer with Malphigiales, for traits thefor assignment freezing of whichconditions. within eudicots is debated (e.g. Zavada & Dilcher, 16; Ekspansio tropiikista kylmään vuodenaikaisilmastoon Malvidae and Fabidae, respectively, is stable. Thus, the Batten, 19; Sims et al., 1999) and so, although there is rehensive view Because evolutionary rates are unlikely support to be(extended uniform 2013nature.htm). Data thistable phylogenetic 4). These This results timetree were generally gives us the robust most comprehensive phenology (6,705view species) Because andliitukauden conduit evolutionary diameter rates (2,181 arealun species). unlikely globaalimuutos be uniform at this phylogenetic constraints are likely to be robust to future phylogenetic good evidence for a relationship of some Normapolles e basis of their scale, we ran growth form analyses both across the yet entire intoangiosperm the evolutionary history of angiosperms. On the basis of their scale, we ran growth formanalyses. analyses both across the entire angiosperm species to crown Fagales (Friis et al., 2006b), it is not The oldest potential evidence for core rosids is unequivocal that all belong to core rosids. Thus, they do cupancies with data set and also within each of four major a lineages: Monocotyledoneae geographic distributions, we classified species climate occupancies with Figure data set 3 and Coordinated also within evolutionary each of four transition major lineages: Monocotyledoneae Normapolles pollen that first appears in the Cenomanian not provide sufficient evidence on which to establish a 17% 32% rates between growth form and Alkujaan puita, joilla laajaonteloiset johtosolukot: tehokkaat, mutta of Europe climate and North America (e.g. Pacltová, 1971; Doyle minimum constraint for the divergence of Fabidae and g temperatures (monocots), Magnoliidae (magnoliids), Superrosidae respect (superrosids) freezing: freezing unexposed, only encountering temperatures (monocots), Magnoliidae (magnoliids), Superrosidae (superrosids) occupancy. a, A representation & Robbins, of coordinated 1977). The precise systematic placement of Malvidae. Angiospermae Woody Herbaceous (N = 12,706) alttiit jäätymiselle ja pakkaselle evolution for the best likelihood-based model [CO between growth form for 12,706 species Ó 2011 The Authors 2 ]-pitoisuus kasvoi nopeasti New Phytologist (2011) 192: % 11% b N = 860 a N = 2,630 b(herbaceous, green; N = 860 woody, brown) New Phytologist andó climate 2011 New Phytologist Trust liitukaudenwww.newphytologist.com alussa: jopa 7.7 C 1 Kapeat occupancy based on a model assuming the same johtosolukot mahdollistivat leviämisen kylmään ilmastoon 24% Transitions per rates 24% were applied to all Angiospermae (top Transitions plot per nousu lämpötilassa 0% 43% million years 16% 18% 2 above the 0% 43% million years dashed arrow), and the best-fit model, in Ruohovartisuus mahdollisti leviämisen kylmään ilmastoon: 1% % 14% 2% 24% 14% 21% 34% 0.01 which rates were estimated separately for the major Merenpinta nousi m, maanpäälliset Small osat conduits Evergreen kuihtuvat Monocot. talveksi Magnoliidae Superrosidae Deciduous lineages, that is, Monocotyledoneae, Magnoliidae, Superasteridae (N = ,873) (N = 532) (N = 4,763) (N = 4,017) Superrosidae and Superasteridae (bottom four syvänteet paljon lämpimämpiä 3 Kausivihannuus 2% 55% mahdollisti selviämisen 5% talven yli kylmässä ilmastossa plots below the dashed arrows). b, The weighted % 82% 3% 59% 59% 3% 7% 37% 9% 2% 55% 1.00 average (by clade diversity) of the relative (+15 C) 14% 14% likelihood of the different pathways out of the woody and freezing-unexposed state and into the Ei napajäätiköitä, mutta ilmasto d herbaceous and freezing-exposed state (see Fig. 2 b c d Woody Large conduits Evergreen Transitions per Persistence time and Methods for further Large conduits details). ilmeisesti vaihtelevaa Persistence time million years (million years) Persistence time (million years) (million years) Large conduits Herbaceous Deciduous Large conduits 10 en 10 Woody Evergreen g ous g en leaf b, A d-based ark green; Trait first 82.7% Simultaneous 0.0% Climate first 17.3% 50 Trait first 58.0% Simultaneous 0.0% Climate first 42.0% Herbaceous defined as the inverse of the sum of the transition rates away Figure from2 acoordinated given Zanne evolutionary et al. (2014) transition Nature rates 506, between leaf character state (that is, the inverse of the sum of all arrow rates phenology out of a character or conduit diameter and climate occupancy. a, b, A 2014 Macmillan Publishers Limited. All rights reserved Jari state). Oksanen c, d, The (Biologia) relative likelihood of the: different pathways Yleiset representation out ofpiirteet the evergreen of coordinated evolution for the 2016 best likelihood-based 27 / 40 and freezing-unexposed state and into the deciduous andmodel freezing-exposed between leaf phenology for 2,630 species (evergreen, dark green; 0.10 Trait first 36.7% Simultaneous 14.6% 80 Climate first 48.7% Deciduous Trait first 82.7% Simultaneous 0.0% Clarke, Warrock & Donoghue (2011) New Phytol 192, Climate first 17.3% 6 F E B R U A RY V O L N AT U R E Pangean pilkkoutuminen nopeaa yhdessä koppisiemenisten radiaation kanssa Vulkaaninen toiminta voimakasta defined as the inverse of the sum of the transition rates away from a given character state (that is, the inverse of the sum of all arrow rates out of a character state). c, d, Jari TheOksanen relative likelihood (Biologia) of the different pathways : out of the evergreen Yleiset piirteet and freezing-unexposed state and into the deciduous and freezing-exposed / 40

7 Koevoluutio: pölytys Koevoluutio: herbivoria Dinosaurusten laidunnus loi vapaita paikkoja laidunnustoleranteille koppisiemenisille? Kukka kehittyi yhdessä hyönteispölytyksen kanssa: lyhyet heteet, vähäinen siitepölymäärä & siitepölyn paakkuuntuminen viittaavat hyönteispölytykseen Hyönteispölytys mahdollistaa tehokkaan geeninvaihdon ilmeisesti myös autoinkompatibiliteetti kehittyi varhain Jari Oksanen (Biologia) : Yleiset piirteet / 40 Turcotte & al, Proc RS 281; Kasvit näkevät paljon vaivaa sekundaariyhdisteiden tuottamiseksi ja niiden kirjo on suuri Yleensä niitä pidetään antiherbivorisina, mutta yksikään klaadi ei ole päässyt pakoon Kasvumuoto on tärkeämpi: puiden lehtiä syödään Keskimäärin 5 % lehdistä syödään vuosittain Jari Oksanen (Biologia) : Yleiset piirteet / 40 Liitukauden lopun kasvillisuus Liitukauden loppu: Suuri ympäristökatastrofi Liitukausi päättyi suuren ympäristökatastrofiin, joka tuhosi dinosaurukset (paitsi linnut) ja aiheutti laajoja sukupuuttoja; liitukausi tertiaari eli K-T -raja geologiassa 1 Meteorin isku Jukataniin tai lähelle? Useampi meteori? Jättimäinen tulivuorenpurkaus Intiassa? Jokin muu katastrofi? Koppisiemenisten nopea radiaatio tertiaarikaudella ei kuitenkaan massasukupuuttoa Tertiaarin alku oli vielä lämmin, mutta mannerten liikkeet avasivat kylmille napavesille tien ja poimuvuoristojen nousu esti ilmamassojen liikkeitä: maapallo kylmeni Myös [CO 2 ]-pitoisuus aleni Nykyään (viimeisten 1.8 milj. vuoden aikana) hyvin kylmää ja jääkaudet yleisiä 1 tertiaari-nimitystä ei enää käytettäne geologiassa vaan puhutaan paleogeenistä. Jari Oksanen (Biologia) : Yleiset piirteet / 40 Jari Oksanen (Biologia) : Yleiset piirteet / 40

8 Lämpötila ja kasvillisuus tertiaarikaudella Heinävaltaisen kasvillisuuden synty Ensimmäiset heinäfossiilit milj. v sitten Heinävaltaisia yhteisöjä alkaen milj. v sitten Nykyisin n lajia, jotka vallitsevina laajoissa heinävaltaisissa yhteisöissä (25 30 % maapinta-alasta) Heinät kestävät kuivuutta, kausikylmyyttä, kuloja ja herbivoriaa Heinien kanssa kehittyivät niitä laiduntamaan pystyvät nisäkkäät (hevosten, kamelien ja antilooppien esi-isät) sekä heinäperhoset Jari Oksanen (Biologia) : Yleiset piirteet / 40 Jari Oksanen (Biologia) : Yleiset piirteet / 40 Heinikoiden synty: fossiilitodisteet C 4 C 4 -kasvit lisäävät tavalliseen fotosynteesiin uuden vaiheen, jossa CO 2 sidotaan nelihiilisiin yhdisteisiin mesofyllissä ja siirretään jännetupen soluihin normaaliin fotoassimilaatioon Tunnusomainen anatominen rakenne, joka voidaan tunnistaa myös fossiileista C 4 -metabolia kehittyi milj. v sitten ja yleistyi n. 7 milj. v sitten C 4 on tehokkaampi kaasumaisen CO 2 :n sitoja ja mahdollistaa yhteytyksen pienemmällä veden haihdutushävikillä: etu kuivissa oloissa Ilmakehän [CO 2 ]-pitoisuuden aleneminen: foto-oksidaatiosta suuremmat tappiot Vaatii kuitenkin korkeampaa lämpötilaa kuin konventionaalinen yhteytys Syntynyt useita kertoja erilaisissa koppisiemenisryhmissä Tärkeimpiä ryhmiä heinät (Poaceae) ja sarat (Cyperaceae) sekä jotkin kaksisirkkaiset Jari Oksanen (Biologia) : Yleiset piirteet / 40 Jari Oksanen (Biologia) : Yleiset piirteet / 40

9 C 4 fylogenia 350 Review Tansley review Mioseenin kasvillisuus Fig. 5 Distribution of C 4 photosynthesis in the taxonomic orders of the angiosperms. Angiosperm orders with C 4 photosynthesis are shown in Jari bold. Oksanen Lines to the (Biologia) right of these orders indicate families : and principal C 4 genera Yleiset within piirteet a lineage. Numbers in parentheses refer to estimates 2016of 39 / 40 genera/species numbers or, where relevant, just species numbers. Adapted from Stevens (2003) by permission. Sage RF (2004) New Phytol 161, Jari Oksanen (Biologia) : Yleiset piirteet / 40 has salsina (suaedoid) Kranz anatomy. The other two C 4 lineages arising from Suaeda are the single-celled C 4 species Bienertia cycloptera and Borszczowia aralocaspica. Nonphotosynthetic characteristics clearly place these species in the Suadoideae tribe of the Chenopodiaceae, while the unique single-celled C 4 anatomy distinguishes them from each other and all other C 4 species, demonstrating independent evolution of the C 4 pathway (Freitag & Stichler, 2002; Schütze et al., 2003). V. Where did C 4 photosynthesis evolve? The identification of the C 4 lineages allows for an assessment of the regions and habitats where C 4 photosynthesis evolved. Centers of C 4 origin are indicated by (1) the geographic distribution of species expressing intermediate traits between C 3 and C 4 photosynthesis; (2) the location of the greatest taxonomic diversity within a C 4 lineage; and (3) the location of the nearest C 3 relatives (Powell, 1978; Pyankov et al., 2001b). This approach works well in the dicots, where most lineages have relatively low diversity and appear to be of recent origin (Ehleringer et al., 1997; Pyankov et al., 2001b). In grasses and sedges, the higher number of species and greater age of the C 4 pathway create a more complex picture and points of origin are uncertain at this time. From the distribution of C 4 dicots and their relatives, it is apparent that the 30 or so lineages are associated with one of five general centers of C 4 diversity that occur in the arid tropics, subtropics and warm temperate zones (Fig. 9). In North America, the main center corresponds to the arid zone stretching from southern Texas into central Mexico. With reasonably high confidence, the origin of five C 4 dicot lineages can be located in this region. In Flaveria, for example, this region has the greatest species and functional type diversity, with C 3, C 4 and most intermediate species (Powell, 1978). In addition, the nearest relative to Flaveria, the genus Sartwellia, occurs in the area. The nearest C 3 relative of C 4 Chamaesyce (Euphorbiaceae) occurs in southern Texas, indicating that C 4 photosynthesis arose here in this group (Webster et al., 1975). C 4 Heliotropium section Orthostachys also appears to have arisen in the Mexican center due to high diversity of this section in northern Mexico and the presence of C 3 C 4 New Phytologist (2004) 161: