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  • 1.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Physiological Botany.
    MADS-Box Gene Phylogeny and the Evolution of Plant Form: Characterisation of a Family of Regulators of Reproductive Development from the Conifer Norway Spruce, Picea abies2002Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    The evolutionary relationships between the angiosperm floral organs and the reproductive organs of other seed plants is not known. Flower organ development requires transcription factors encoded by the MADS-box genes. Since the evolution of novel morphology likely involve changes in developmental regulators, I have analysed MADS-box genes from the conifer Norway spruce, Picea abies, a representative of the gymnosperm group of seed plants.

    The results show that the MADS-box gene family has evolved via gene duplications and subsequent diversifications in correlation in time with the evolution of morphological novelties along the seed-plant lineage.

    Angiosperm MADS-box genes that determine petal and stamen development have homologues in the conifers, that are specifically active in pollen cones. It is, therefore, likely that the common ancestor of these genes controlled the development of the pollen-bearing organs in the early seed plants, and later were recruited for petal development in the angiosperms.

    Norway spruce set cones at an age of 15-20 years. One of the spruce MADS-box genes analysed may have a function in the control of the transition to reproductive phase, supported by expression data and the effect of the gene on development of transgenic Arabidopsis plants.

    Two of the spruce genes identified are not closely related to any known angiosperm gene. These may have roles in gymnosperm-specific developmental processes, possibly in the patterning of the conifer cones, as suggested by their expression patterns.

    The molecular regulation of cone- and flower development in fundamental aspects is highly conserved between conifers and angiosperms, however, differences detected may be informative regarding the origin of morphological complexity.

    List of papers
    1. MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B-class floral homeotic genes in angiosperms
    Open this publication in new window or tab >>MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B-class floral homeotic genes in angiosperms
    Show others...
    1999 (English)In: Developmental Genetics, ISSN 0192-253X, E-ISSN 1520-6408, Vol. 25, no 3, p. 253-266Article in journal (Refereed) Published
    Abstract [en]

    The reproductive organs of conifers, the pollen cones and seed cones, differ in morphology from the angiosperm flower in several fundamental respects. In this report we present evidence to suggest that the two plant groups, in spite of these morphological differences and the long evolutionary distance between them, share important features in regulating the development of the reproductive organs. We present the cloning of three genes, DAL11, DAL12, and DAL13, from Norway spruce, all of which are related to the angiosperm B-class of homeotic genes. The B-class genes determine the identities of petals and stamens. They are members of a family of MADS-box genes, which also includes C-class genes that act to determine the identity of carpels and, in concert with B genes specify stamens in the angiosperm flower. Phylogenetic analyses and the presence of B-class specific C-terminal motifs in the DAL protein sequences imply homology to the B-class genes. Specific expression of all three genes in developing pollen cones suggests that the genes are involved in one aspect of B function, the regulation of development of the pollen-bearing organs. The different temporal and spatial expression patterns of the three DAL genes in the developing pollen cones indicate that the genes have attained at least in part distinct functions. The DAL11, DAL12, and 13 expression patterns in the pollen cone partly overlap with that of the previously identified DAL2 gene, which is structurally and functionally related to the angiosperm C-class genes. This result supports the hypothesis that an interaction between B- and C-type genes is required for male organ development in conifers like in the angiosperms. Taken together, our data suggests that central components in the regulatory mechanisms for reproductive organ development are conserved between conifers and angiosperms and, thus, among all seed plants.

    National Category
    Natural Sciences
    Identifiers
    urn:nbn:se:uu:diva-89833 (URN)10.1002/(SICI)1520-6408(1999)25:3<253::AID-DVG8>3.0.CO;2-P (DOI)10528266 (PubMedID)
    Note

    De två första författarna delar förstaförfattarskapet.

    Available from: 2002-04-29 Created: 2002-04-29 Last updated: 2017-12-14Bibliographically approved
    2. The DAL10 gene from Norway spruce Picea abies belongs to a potentially gymnosperm-specific subgroup of MADS-box genes and is specifically active in seed- and pollen cones
    Open this publication in new window or tab >>The DAL10 gene from Norway spruce Picea abies belongs to a potentially gymnosperm-specific subgroup of MADS-box genes and is specifically active in seed- and pollen cones
    Show others...
    Manuscript (Other academic)
    Identifiers
    urn:nbn:se:uu:diva-89834 (URN)
    Available from: 2002-04-29 Created: 2002-04-29 Last updated: 2016-04-25Bibliographically approved
    3. The MADS-box gene DAL1 is a potential mediator of the juvenile to adult transition in the conifer Norway spruce, Picea abies
    Open this publication in new window or tab >>The MADS-box gene DAL1 is a potential mediator of the juvenile to adult transition in the conifer Norway spruce, Picea abies
    Show others...
    Manuscript (Other academic)
    Identifiers
    urn:nbn:se:uu:diva-89835 (URN)
    Available from: 2002-04-29 Created: 2002-04-29 Last updated: 2016-04-25Bibliographically approved
    4. Evolutionary diversification of the MADS-box gene family; an analysis of nine novel genes from the conifer Norway spruce
    Open this publication in new window or tab >>Evolutionary diversification of the MADS-box gene family; an analysis of nine novel genes from the conifer Norway spruce
    Manuscript (Other academic)
    Identifiers
    urn:nbn:se:uu:diva-89836 (URN)
    Available from: 2002-04-29 Created: 2002-04-29 Last updated: 2016-04-25Bibliographically approved
  • 2.
    Carlsbecker, Annelie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics. fysiologisk botanik.
    Helariutta, Y
    Phloem and xylem specification: pieces of the puzzle emerge2005In: Current Opinion in Plant Biology, Vol. 8, no 5, p. 512-517Article in journal (Refereed)
    Abstract [en]

    The plant vascular system is composed of two tissue types, xylem and phloem, which originate from the vascular meristem, the procambium. Recently, several regulatory mechanisms that control the specification of these two tissue types have been uncovered. These include the asymmetric patterning of xylem and phloem in the vascular bundle by the class III HD-ZIP and KANADI genes, the tissue-type-specific control of vascular cell proliferation by brassinosteroids and class III HD-ZIP genes, the regulation of vascular tissue identity by the MYB-like transcription factor APL, and inductive signalling during xylem differentiation by xylogen. These findings define an emerging developmental framework for the control of vascular tissue specification.

  • 3.
    Carlsbecker, Annelie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Physiological Botany.
    Izquierdo, Liz
    Sundström, Jens
    Engström, Peter
    Evolutionary diversification of the MADS-box gene family; an analysis of nine novel genes from the conifer Norway spruceManuscript (Other academic)
  • 4.
    Carlsbecker, Annelie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Physiological Botany.
    Lee, Ji-Young
    Roberts, Christina J.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Physiological Botany.
    Dettmer, Jan
    Lehesranta, Satu
    Zhou, Jing
    Lindgren, Ove
    Moreno-Risueno, Miguel A.
    Vatén, Anne
    Thitamadee, Siripong
    Campilho, Ana
    Sebastian, Jose
    Bowman, John L.
    Helariutta, Yka
    Benfey, Philip N.
    Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate2010In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 465, no 7296, p. 316-321Article in journal (Refereed)
    Abstract [en]

    A key question in developmental biology is how cells exchange positional information for proper patterning during organ development. In plant roots the radial tissue organization is highly conserved with a central vascular cylinder in which two water conducting cell types, protoxylem and metaxylem, are patterned centripetally. We show that this patterning occurs through crosstalk between the vascular cylinder and the surrounding endodermis mediated by cell-to-cell movement of a transcription factor in one direction and microRNAs in the other. SHORT ROOT, produced in the vascular cylinder, moves into the endodermis to activate SCARECROW. Together these transcription factors activate MIR165a and MIR166b. Endodermally produced microRNA165/6 then acts to degrade its target mRNAs encoding class III homeodomain-leucine zipper transcription factors in the endodermis and stele periphery. The resulting differential distribution of target mRNA in the vascular cylinder determines xylem cell types in a dosage-dependent manner.

  • 5.
    Carlsbecker, Annelie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Sundstrom, Jens F.
    Englund, Marie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Uddenberg, Daniel
    Izquierdo, Liz
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology.
    Kvarnheden, Anders
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology.
    Vergara-Silva, Francisco
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Molecular control of normal and acrocona mutant seed cone development in Norway spruce (Picea abies) and the evolution of conifer ovule-bearing organs2013In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 200, no 1, p. 261-275Article in journal (Refereed)
    Abstract [en]

    Reproductive organs in seed plants are morphologically divergent and their evolutionary history is often unclear. The mechanisms controlling their development have been extensively studied in angiosperms but are poorly understood in conifers and other gymnosperms. Here, we address the molecular control of seed cone development in Norway spruce, Picea abies. We present expression analyses of five novel MADS-box genes in comparison with previously identified MADS and LEAFY genes at distinct developmental stages. In addition, we have characterized the homeotic transformation from vegetative shoot to female cone and associated changes in regulatory gene expression patterns occurring in the acrocona mutant. The analyses identified genes active at the onset of ovuliferous and ovule development and identified expression patterns marking distinct domains of the ovuliferous scale. The reproductive transformation in acrocona involves the activation of all tested genes normally active in early cone development, except for an AGAMOUS-LIKE6/SEPALLATA (AGL6/SEP) homologue. This absence may be functionally associated with the nondeterminate development of the acrocona ovule-bearing scales. Our morphological and gene expression analyses give support to the hypothesis that the modern cone is a complex structure, and the ovuliferous scale the result of reductions and compactions of an ovule-bearing axillary short shoot in cones of Paleozoic conifers.

  • 6.
    Carlsbecker, Annelie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Physiological Botany.
    Sundström, Jens
    Tandre, Karolina
    Englund, Marie
    Kvarnheden, Anders
    Johanson, Urban
    Engström, Peter
    The DAL10 gene from Norway spruce Picea abies belongs to a potentially gymnosperm-specific subgroup of MADS-box genes and is specifically active in seed- and pollen conesManuscript (Other academic)
  • 7.
    Carlsbecker, Annelie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Sundström, Jens
    Tandre, Karolina
    Englund, Marie
    Kvarnheden, Anders
    Johansson, Urban
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    The DAL10 gene from Norway spruce (Picea abies) belongs to a potentially gymnosperm-specific subclass of MADS-box genes and is specifically active in seed cones and pollen cones.2003In: Evolution & Development, Vol. 5, no 6, p. 551-561Article in journal (Refereed)
  • 8.
    Carlsbecker, Annelie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Physiological Botany.
    Tandre, Karolina
    Johanson, Urban
    Englund, Marie
    Engström, Peter
    The MADS-box gene DAL1 is a potential mediator of the juvenile to adult transition in the conifer Norway spruce, Picea abiesManuscript (Other academic)
  • 9.
    Carlsbecker, Annelie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Fysiologisk botanik.
    Tandre, Karolina
    Johansson, Urban
    Englund, Marie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Fysiologisk botanik.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Fysiologisk botanik.
    The MADS-box gene DAL1 is a potential mediator of the juvenile-to-adult transition in Norway spruce (Picea abies)2004In: The Plant Journal, Vol. 40, p. 546-557Article in journal (Refereed)
    Abstract [en]

    Progression through the plant life cycle involves changes in many essential features, most notably in the capacity to reproduce. The transition from juvenile vegetative and non-reproductive to an adult reproductive phase is gradual and can take many years; in the conifer Norway spruce, Picea abiea, typically 20-25 years. We present a detailed analysis of the activities of three regulatory genes with potential roles in the transition in Norway spruce: DAL1, a MADS-box gene related to the AGL6 group of genes from angiosperms, and the two LEAFY-related genes PaLFY and PaNLY. DAL1 activity is initiated in the shoots of juvenile trees at an age of 3-5 years, and then increases with age, whereas both LFY genes are active throughout the juvenile phase. The activity of DAL1 further shows a spatial pattern along the stem of the tree that parallels a similar gradient in physiolpoical and morphological features associated with maturation to the adult phase. Constitutive expression of DAL1 in transgenic Arabidopsis plants caused a dramatic attenuation of both juvenile and adult growth phases;flowers forming immediately after the embryogenic phase of development in severely affected plants. Taken together, our resulsts support the notion that DAL1 may have a regulatory role in the juvenile-to-adult transition in Norway spruce.

  • 10. de Vries, Jan
    et al.
    Fischer, Angela Melanie
    Roettger, Mayo
    Rommel, Sophie
    Schluepmann, Henriette
    Bräutigam, Andrea
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Gould, Sven Bernhard
    Cytokinin-induced promotion of root meristem size in the fern Azolla supports a shoot-like origin of euphyllophyte roots.2016In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 209, no 2, p. 705-720Article in journal (Refereed)
    Abstract [en]

    The phytohormones cytokinin and auxin orchestrate the root meristem development in angiosperms by determining embryonic bipolarity. Ferns, having the most basal euphyllophyte root, form neither bipolar embryos nor permanent embryonic primary roots but rather an adventitious root system. This raises the questions of how auxin and cytokinin govern fern root system architecture and whether this can tell us something about the origin of that root. Using Azolla filiculoides, we characterized the influence of IAA and zeatin on adventitious fern root meristems and vasculature by Nomarski microscopy. Simultaneously, RNAseq analyses, yielding 36 091 contigs, were used to uncover how the phytohormones affect root tip gene expression. We show that auxin restricts Azolla root meristem development, while cytokinin promotes it; it is the opposite effect of what is observed in Arabidopsis. Global gene expression profiling uncovered 145 genes significantly regulated by cytokinin or auxin, including cell wall modulators, cell division regulators and lateral root formation coordinators. Our data illuminate both evolution and development of fern roots. Promotion of meristem size through cytokinin supports the idea that root meristems of euphyllophytes evolved from shoot meristems. The foundation of these roots was laid in a postembryonically branching shoot system.

  • 11.
    Englund, Marie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Vergara-Silva, Francisco
    Morphological "primary homology" and expression of AG -subfamily MADS-box genes in pines, podocarps, and yews2011In: Evolution & Development, ISSN 1520-541X, E-ISSN 1525-142X, Vol. 13, no 2, p. 171-181Article in journal (Refereed)
    Abstract [en]

    The morphological variation among reproductive organs of extant gymnosperms is remarkable, especially among conifers. Several hypotheses concerning morphological homology between various conifer reproductive organs have been put forward, in particular in relation to the pine ovuliferous scale. Here, we use the expression patterns of orthologs of the ABC-model MADS-box gene AGAMOUS (AG) for testing morphological homology hypotheses related to organs of the conifer female cone. To this end, we first developed a tailored 3'RACE procedure that allows reliable amplification of partial sequences highly similar to gymnosperm-derived members of the AG-subfamily of MADS-box genes. Expression patterns of two novel conifer AG orthologs cloned with this procedure-namely PodAG and TgAG, obtained from the podocarp Podocarpus reichei and the yew Taxus globosa, respectively-are then further characterized in the morphologically divergent female cones of these species. The expression patterns of PodAG and TgAG are compared with those of DAL2, a previously discovered Picea abies (Pinaceae) AG ortholog. By treating the expression patterns of DAL2, PodAG, and TgAG as character states mapped onto currently accepted cladogram topologies, we suggest that the epimatium-that is, the podocarp female cone organ previously postulated as a "modified" ovuliferous scale-and the canonical Pinaceae ovuliferous scale can be legitimally conceptualized as "primary homologs." Character state mapping for TgAG suggests in turn that the aril of Taxaceae should be considered as a different type of organ. This work demonstrates how the interaction between developmental-genetic data and formal cladistic theory could fruitfully contribute to gymnosperm systematics.

  • 12.
    Englund, Marie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Vergara-Silva, Francisco
    Morphological "primary homology" and expression of AG -subfamily MADS-box genes in pines, podocarps, and yews2011In: Evolution & Development, ISSN 1520-541X, E-ISSN 1525-142X, Vol. 13, no 2, p. 171-181Article in journal (Refereed)
    Abstract [en]

    The morphological variation among reproductive organs of extant gymnosperms is remarkable, especially among conifers. Several hypotheses concerning morphological homology between various conifer reproductive organs have been put forward, in particular in relation to the pine ovuliferous scale. Here, we use the expression patterns of orthologs of the ABC-model MADS-box gene AGAMOUS (AG) for testing morphological homology hypotheses related to organs of the conifer female cone. To this end, we first developed a tailored 3'RACE procedure that allows reliable amplification of partial sequences highly similar to gymnosperm-derived members of the AG-subfamily of MADS-box genes. Expression patterns of two novel conifer AG orthologs cloned with this procedure-namely PodAG and TgAG, obtained from the podocarp Podocarpus reichei and the yew Taxus globosa, respectively-are then further characterized in the morphologically divergent female cones of these species. The expression patterns of PodAG and TgAG are compared with those of DAL2, a previously discovered Picea abies (Pinaceae) AG ortholog. By treating the expression patterns of DAL2, PodAG, and TgAG as character states mapped onto currently accepted cladogram topologies, we suggest that the epimatium-that is, the podocarp female cone organ previously postulated as a "modified" ovuliferous scale-and the canonical Pinaceae ovuliferous scale can be legitimally conceptualized as "primary homologs." Character state mapping for TgAG suggests in turn that the aril of Taxaceae should be considered as a different type of organ. This work demonstrates how the interaction between developmental-genetic data and formal cladistic theory could fruitfully contribute to gymnosperm systematics.

  • 13.
    Groth, Erika
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Tandre, Karolina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Functional divergence by multiple mechanisms between the paralogous sister genes DAL1 and DAL14 in the AGL6 subfamily of MADS-box genes in the conifer Picea abiesManuscript (preprint) (Other academic)
  • 14.
    Müller, Christina Joy
    et al.
    Swedish Univ Agr Sci, Dept Plant Biol, Uppsala BioCtr, Ulls Vag 24E, SE-75651 Uppsala, Sweden.;Swedish Univ Agr Sci, Linnean Ctr Plant Biol Uppsala, Ulls Vag 24E, SE-75651 Uppsala, Sweden..
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Wang, Guodong
    Shaanxi Normal Univ, Minist Educ Med Plant Resource & Nat Pharmaceut C, Natl Engn Lab Resource Dev Endangered Chinese Cru, Key Lab,Coll Life Sci, Xian 710062, Peoples R China..
    Ramachandran, Prashanth
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Beste, Lisa
    Institutionen för växtproduktionsekologi, SLU, Uppsala.
    Uddenberg, Daniel
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    PHABULOSA Mediates an Auxin Signaling Loop to Regulate Vascular Patterning in Arabidopsis2016In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 170, no 2, p. 956-970Article in journal (Refereed)
    Abstract [en]

    Plant vascular tissues, xylem and phloem, differentiate in distinct patterns from procambial cells as an integral transport system for water, sugars, and signaling molecules. Procambium formation is promoted by high auxin levels activating class III homeodomain leucine zipper (HD-ZIP III) transcription factors (TFs). In the root of Arabidopsis (Arabidopsis thaliana), HD-ZIP III TFs dose-dependently govern the patterning of the xylem axis, with higher levels promoting metaxylem cell identity in the central axis and lower levels promoting protoxylem at its flanks. It is unclear, however, by what mechanisms the HD-ZIP III TFs control xylem axis patterning. Here, we present data suggesting that an important mechanism is their ability to moderate the auxin response. We found that changes in HD-ZIP III TF levels affect the expression of genes encoding core auxin response molecules. We show that one of the HD-ZIP III TFs, PHABULOSA, directly binds the promoter of both MONOPTEROS (MP)/AUXIN RESPONSE FACTOR5, a key factor in vascular formation, and IAA20, encoding an auxin/indole acetic acid protein that is stable in the presence of auxin and able to interact with and repress MP activity. The double mutant of IAA20 and its closest homolog IAA30 forms ectopic protoxylem, while overexpression of IAA30 causes discontinuous protoxylem and occasional ectopic metaxylem, similar to a weak loss-of-function mp mutant. Our results provide evidence that HD-ZIP III TFs directly affect the auxin response and mediate a feed-forward loop formed by MP and IAA20 that may focus and stabilize the auxin response during vascular patterning and the differentiation of xylem cell types.

  • 15.
    Nilsson, Lars
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Physiological Botany.
    Sundås Larsson, Annika
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Physiological Botany.
    Vahala, Tiina
    APETALA2 like genes from Picea abies show functional similarities to their Arabidopsis homologues2007In: Planta, ISSN 0032-0935, E-ISSN 1432-2048, Vol. 225, no 3, p. 589-602Article in journal (Refereed)
    Abstract [en]

    In angiosperm flower development the identity of the floral organs is determined by the A, B and C factors. Here we present the characterisation of three homologues of the A class gene APETALA2 (AP2) from the conifer Picea abies (Norway spruce), Picea abies APETALA2 LIKE1 (PaAP2L1), PaAP2L2 and PaAP2L3. Similar to AP2 these genes contain sequence motifs complementary to miRNA172 that has been shown to regulate AP2 in Arabidopsis. The genes display distinct expression patterns during plant development; in the female-cone bud PaAP2L1 and PaAP2L3 are expressed in the seed-bearing ovuliferous scale in a pattern complementary to each other, and overlapping with the expression of the C class-related gene DAL2. To study the function of PaAP2L1 and PaAP2L2 the genes were expressed in Arabidopsis. The transgenic PaAP2L2 plants were stunted and flowered later than control plants. Flowers were indeterminate and produced an excess of floral organs most severely in the two inner whorls, associated with an ectopic expression of the meristem-regulating gene WUSCHEL. No homeotic changes in floral-organ identities occurred, but in the ap2-1 mutant background PaAP2L2 was able to promote petal identity, indicating that the spruce AP2 gene has the capacity to substitute for an A class gene in Arabidopsis. In spite of the long evolutionary distance between angiosperms and gymnosperms and the fact that gymnosperms lack structures homologous to sepals and petals our data supports a functional conservation of AP2 genes among the seed plants.

  • 16.
    Ramachandran, Prashanth
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Etchells, J. Peter
    Univ Durham, Dept Biosci, South Rd, Durham DH1 3LE, England..
    Class III HD- ZIPs govern vascular cell fate: an HD view on patterning and differentiation2017In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 68, no 1, p. 55-69Article, review/survey (Refereed)
    Abstract [en]

    Plant vasculature is required for the transport of water and solutes throughout the plant body. It is constituted of xylem, specialized for transport of water, and phloem, that transports photosynthates. These two differentiated tissues are specified early in development and arise from divisions in the procambium, which is the vascular meristem during primary growth. During secondary growth, the xylem and phloem are further expanded via differentiation of cells derived from divisions in the cambium. Almost all of the developmental fate decisions in this process, including vascular specification, patterning, and differentiation, are regulated by transcription factors belonging to the class III homeodomain-leucine zipper (HD-ZIP III) family. This review draws together the literature describing the roles that these genes play in vascular development, looking at how HD-ZIP IIIs are regulated, and how they in turn influence other regulators of vascular development. Themes covered vary, from interactions between HD-ZIP IIIs and auxin, cytokinin, and brassinosteroids, to the requirement for exquisite spatial and temporal regulation of HD-ZIP III expression through miRNA-mediated post-transcriptional regulation, and interactions with other transcription factors. The literature described places the HD-ZIP III family at the centre of a complex network required for initiating and maintaining plant vascular tissues.

  • 17.
    Ramachandran, Prashanth
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden.
    Wang, Guodong
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden.
    Augstein, Frauke
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden.
    de Vries, Jan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden, Canada..
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden.
    Continuous root xylem formation and vascular acclimation to water deficit involves endodermal ABA signalling via miR1652018In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 145, no 3, article id dev159202Article in journal (Refereed)
    Abstract [en]

    The plant root xylem comprises a specialized tissue for water distribution to the shoot. Despite its importance, its potential morphological plasticity in response to environmental conditions such as limited water availability has not been thoroughly studied. Here, we identify a role for the phytohormone abscisic acid (ABA) for proper xylem development and describe how ABA signalling-mediated effects on core developmental regulators are employed to alter xylem morphology under limited water availability in Arabidopsis. Plants with impaired ABA biosynthesis and reduced ABA signalling in the cell layer surrounding the vasculature displayed defects in xylem continuity, suggesting that non-cell autonomous ABA signalling is required for proper xylem development. Conversely, upon external ABA application or under limited water availability, extra xylem strands were formed. The observed xylem developmental alterations were dependent on adequate endodermal ABA signalling, which activated MIR165A. This resulted in increased miR165 levels that repress class III HD-ZIP transcription factors in the stele. We conclude that a pathway known to control core developmental features is employed as a means of modifying plant xylem morphology under conditions of environmental stress.

  • 18.
    Roberts, Christina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Help, Hanna
    Institute of Biotecnology, University of Helsinki, Finland.
    Helariutta, Ykä
    Institute of Biotecnology, University of Helsinki, Finland.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Class III HD-ZIP Transcription Factors Regulate Auxin Signalling to Pattern Arabidopsis Root VasculatureManuscript (preprint) (Other academic)
  • 19.
    Roberts, Christina Joy
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Class III HD-ZIP transcription factors control root growth and vascular patterning2013Conference paper (Other academic)
  • 20.
    Roberts, Christina Joy
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology.
    Mechanisms of root growth and vascular patterning regulation by the class III HD-ZIP transcription factors2013Conference paper (Other academic)
  • 21.
    Roberts, Christina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Class III HD-Zip transcription factors control root growth and vascular patterning2013Conference paper (Other academic)
  • 22.
    Roberts, Christina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology.
    Class III HD-ZIP transcription factors control root growth and vascular patterning2012Conference paper (Other academic)
  • 23.
    Roberts, Christina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Class III HD-ZIP Transcription Factors Determine Root Meristem Size by Controlling Reactive Oxygen Species LevelsManuscript (preprint) (Other academic)
  • 24.
    Roberts, Christina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    HD-Zip Class III Transcription factors control root growth and vascular patterning2012Conference paper (Other academic)
    Abstract [en]

    Plants take up water and mineral nutrients through their roots, and this is then distributed throughout the plant via the vascular tissues. Hence, root growth and vascular patterning and differentiation are likely intimately connected to optimize water and nutrient uptake. Mutants defective in the developmental control regulators encoded by Class III homeodomain leucine zipper (HD-ZIP III) genes display alterations both in root growth rates and in vascular patterning. In the wild-type root, the water conducting strands are invariantly patterned such that protoxylem, with spiral or annular secondary walls, occupies peripheral positions in the vascular stele, and metaxylem, characterized by reticulate or pitted secondary walls, are found in central positions. This pattern is altered by mutations in the HD-ZIP III genes: the phb-7d gain-of-function mutant has metaxylem also in protoxylem position, while the athb8 cna phb phv quadruple loss-of-function mutant develops protoxylem in both central and peripheral positions. We have recently shown that the miR165/166 targeting the HD-ZIP III genes moves from the surrounding endodermal cell layer to control the levels of the HD-ZIP III factors in the stele, and that xylem cell fate is dependent on HD-ZIP III levels; high levels specify metaxylem and low levels specify protoxylem (Carlsbecker et al. Nature, 465(7296):316-21, 2010). Similarly, the levels of HD-ZIP III factors appear to determine both root growth rate and meristem size. While phb-7d has a short root and small root apical meristem, the athb8 cna phb phv quadruple mutant has a long root and large apical meristem. To determine what genes are under the control of the HD-ZIP III transcription factors in the root meristem, we have conducted analyses of transcriptome changes upon either inducing a gain-of-function allele of PHB or inducing miR165 to reduce HD-ZIP III levels. Our analyses suggest that the HD-ZIP III transcription factors act upstream of secondary cell wall and programmed cell death control genes, consistent with the observed xylem phenotypes, but are also upstream of a genetic pathway controlling meristem size and growth rate. Hence, the HD-ZIP III transcription factors may act to integrate root growth control and vascular patterning.

  • 25.
    Sundström, Jens
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Physiological Botany.
    Svensson, Mats E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Physiological Botany.
    Svenson, Marie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Physiological Botany.
    Johanson, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Physiological Botany.
    MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B-class floral homeotic genes in angiosperms1999In: Developmental Genetics, ISSN 0192-253X, E-ISSN 1520-6408, Vol. 25, no 3, p. 253-266Article in journal (Refereed)
    Abstract [en]

    The reproductive organs of conifers, the pollen cones and seed cones, differ in morphology from the angiosperm flower in several fundamental respects. In this report we present evidence to suggest that the two plant groups, in spite of these morphological differences and the long evolutionary distance between them, share important features in regulating the development of the reproductive organs. We present the cloning of three genes, DAL11, DAL12, and DAL13, from Norway spruce, all of which are related to the angiosperm B-class of homeotic genes. The B-class genes determine the identities of petals and stamens. They are members of a family of MADS-box genes, which also includes C-class genes that act to determine the identity of carpels and, in concert with B genes specify stamens in the angiosperm flower. Phylogenetic analyses and the presence of B-class specific C-terminal motifs in the DAL protein sequences imply homology to the B-class genes. Specific expression of all three genes in developing pollen cones suggests that the genes are involved in one aspect of B function, the regulation of development of the pollen-bearing organs. The different temporal and spatial expression patterns of the three DAL genes in the developing pollen cones indicate that the genes have attained at least in part distinct functions. The DAL11, DAL12, and 13 expression patterns in the pollen cone partly overlap with that of the previously identified DAL2 gene, which is structurally and functionally related to the angiosperm C-class genes. This result supports the hypothesis that an interaction between B- and C-type genes is required for male organ development in conifers like in the angiosperms. Taken together, our data suggests that central components in the regulatory mechanisms for reproductive organ development are conserved between conifers and angiosperms and, thus, among all seed plants.

  • 26. Uddenberg, Daniel
    et al.
    Akhter, Shirin
    Ramachandran, Prashanth
    Sundström, Jens F
    Carlsbecker, Annelie
    Sequenced genomes and rapidly emerging technologies pave the way for conifer evolutionary developmental biology.2015In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 6Article in journal (Refereed)
    Abstract [en]

    Conifers, Ginkgo, cycads and gnetophytes comprise the four groups of extant gymnosperms holding a unique position of sharing common ancestry with the angiosperms. Comparative studies of gymnosperms and angiosperms are the key to a better understanding of ancient seed plant morphologies, how they have shifted over evolution to shape modern day species, and how the genes governing these morphologies have evolved. However, conifers and other gymnosperms have been notoriously difficult to study due to their long generation times, inaccessibility to genetic experimentation and unavailable genome sequences. Now, with three draft genomes from spruces and pines, rapid advances in next generation sequencing methods for genome wide expression analyses, and enhanced methods for genetic transformation, we are much better equipped to address a number of key evolutionary questions relating to seed plant evolution. In this mini-review we highlight recent progress in conifer developmental biology relevant to evo-devo questions. We discuss how genome sequence data and novel techniques might allow us to explore genetic variation and naturally occurring conifer mutants, approaches to reduce long generation times to allow for genetic studies in conifers, and other potential upcoming research avenues utilizing current and emergent techniques. Results from developmental studies of conifers and other gymnosperms in comparison to those in angiosperms will provide information to trace core molecular developmental control tool kits of ancestral seed plants, but foremost they will greatly improve our understanding of the biology of conifers and other gymnosperms in their own right.

  • 27. Ursache, Robertas
    et al.
    Miyashima, Shunsuke
    Chen, Qingguo
    Vaten, Anne
    Nakajima, Keiji
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Zhao, Yunde
    Helariutta, Yka
    Dettmer, Jan
    Tryptophan-dependent auxin biosynthesis is required for HD-ZIP III-mediated xylem patterning2014In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 141, no 6, p. 1250-1260Article in journal (Refereed)
    Abstract [en]

    The development and growth of higher plants is highly dependent on the conduction of water and minerals throughout the plant by xylem vessels. In Arabidopsis roots the xylem is organized as an axis of cell files with two distinct cell fates: the central metaxylem and the peripheral protoxylem. During vascular development, high and low expression levels of the class III HD-ZIP transcription factors promote metaxylem and protoxylem identities, respectively. Protoxylem specification is determined by both mobile, ground tissue-emanating miRNA165/6 species, which downregulate, and auxin concentrated by polar transport, which promotes HD-ZIP III expression. However, the factors promoting high HD-ZIP III expression for metaxylem identity have remained elusive. We show here that auxin biosynthesis promotes HD-ZIP III expression and metaxylem specification. Several auxin biosynthesis genes are expressed in the outer layers surrounding the vascular tissue in Arabidopsis root and downregulation of HD-ZIP III expression accompanied by specific defects in metaxylem development is seen in auxin biosynthesis mutants, such as trp2-12, wei8 tar2 or a quintuple yucca mutant, and in plants treated with L-kynurenine, a pharmacological inhibitor of auxin biosynthesis. Some of the patterning defects can be suppressed by synthetically elevated HD-ZIP III expression. Taken together, our results indicate that polar auxin transport, which was earlier shown to be required for protoxylem formation, is not sufficient to establish a proper xylem axis but that root-based auxin biosynthesis is additionally required.

  • 28.
    Valdés, Ana Elisa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Roberts, Christina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    HD-Zip class III transcription factors control root development through the modulation of ROS levels2013Conference paper (Other academic)
    Abstract [en]

    In the Arabidopsis root the distinct spatial distribution of two ROS species, hydrogen peroxide and superoxide, controls a dynamic balance between cell division and cell differentiation. Superoxide accumulates in the root meristem while hydrogen peroxide accumulates in the elongation and differentiation zone. The balance between both species controls cell proliferation. Mutants defective in the developmental control regulators encoded by Class III homeodomain leucine zipper (HD-ZIP III) genes display alterations both in root growth rates and levels of ROS species. A gain-of-function mutant of the PHB HD-Zip III gene presents a short root length and small meristem size, while the multiple loss of HD-Zip genes functionality results in bigger root meristem size. Additionally, gain- and loss-of function mutants present contrasting ROS balances. Our analyses of transcriptome changes upon depleting HD-Zip III levels suggest that the HD-Zip class III transcription factors act upstream of ROS-related genetic pathways controlling meristem size and growth rate. Thus, the HD-Zip transcription factors may act to control root growth, possibly by modulation of ROS levels.

  • 29. Vaten, Anne
    et al.
    Dettmer, Jan
    Wu, Shuang
    Stierhof, York-Dieter
    Miyashima, Shunsuke
    Yadav, Shri Ram
    Roberts, Christina J.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Campilho, Ana
    Bulone, Vincent
    Lichtenberger, Raffael
    Lehesranta, Satu
    Mahonen, Ari Pekka
    Kim, Jae-Yean
    Jokitalo, Eija
    Sauer, Norbert
    Scheres, Ben
    Nakajima, Keiji
    Carlsbecker, Annelie
    Gallagher, Kimberly L.
    Helariutta, Yka
    Callose Biosynthesis Regulates Symplastic Trafficking during Root Development2011In: Developmental Cell, ISSN 1534-5807, E-ISSN 1878-1551, Vol. 21, no 6, p. 1144-1155Article in journal (Refereed)
    Abstract [en]

    Plant cells are connected through plasmodesmata (PD), membrane-lined channels that allow symplastic movement of molecules between cells. However, little is known about the role of PD-mediated signaling during plant morphogenesis. Here, we describe an Arabidopsis gene, CALS3/GSL12. Gain-of-function mutations in CALS3 result in increased accumulation of callose (beta-1,3-glucan) at the PD, a decrease in PD aperture, defects in root development, and reduced intercellular trafficking. Enhancement of CALS3 expression during phloem development suppressed loss-of-function mutations in the phloem abundant callose synthase, CALS7 indicating that CALS3 is a bona fide callose synthase. CALS3 alleles allowed us to spatially and temporally control the PD aperture between plant tissues. Using this tool, we are able to show that movement of the transcription factor SHORT-ROOT and microRNA1 65 between the stele and the endodermis is PD dependent. Taken together, we conclude that regulated callose biosynthesis at PD is essential for cell signaling.

  • 30.
    Vázquez-Lobo, Alejandra
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Physiological Botany.
    Vergara-Silva, Fransisco
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Physiological Botany.
    Alvarez-Buylla, Elena R.
    Piñero, Daniel
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Physiological Botany.
    Characterization of the expression patterns of LEAFY/FLORICAULA and NEEDLY orthologs in female and male cones of the conifer genera Picea, Podocarpus, and Taxus: Implications for current evo-devo hypotheses for gymnosperms2007In: Evolution & Development, ISSN 1520-541X, E-ISSN 1525-142X, Vol. 9, no 5, p. 446-459Article in journal (Refereed)
    Abstract [en]

    The identity of genes causally implicated in the development and evolutionary origin of reproductive characters in gymnosperms is largely unknown. Working within the framework of plant evolutionary developmental biology, here we have cloned, sequenced, performed phylogenetic analyses upon and tested the expression patterns of LEAFY/FLORICAULA and NEEDLY orthologs in reproductive structures from selected species of the conifer genera Picea, Podocarpus, and Taxus. Contrary to expectations based on previous assessments, expression of LFY/FLO and NLY in cones of these taxa was found to occur simultaneously in a single reproductive axis, initially overlapping but later in mutually exclusive primordia and/or groups of developing cells in both female and male structures. These observations directly affect the status of the "mostly male theory" for the origin of the angiosperm flower. On the other hand, comparative spatiotemporal patterns of the expression of these genes suggest a complex genetic regulatory network of cone development, as well as a scheme of functional divergence for LFY/FLO with respect to NLY homologs in gymnosperms, both with clear heterochronic aspects. Results presented in this study contribute to the understanding of the molecular-genetic basis of morphological evolution in conifer cones, and may aid in establishing a foundation for gymnosperm-specific, testable evo-devo hypotheses.

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