From Shoot to Leaf: Step-Wise Shifts in Meristem and KNOX1 Activity Correlate with the Evolution of a Unifoliate Body Plan in Gesneriaceae
Total Page：16
File Type：pdf, Size：1020Kb
Dev Genes Evol (2017) 227:41–60 DOI 10.1007/s00427-016-0568-x ORIGINAL ARTICLE From shoot to leaf: step-wise shifts in meristem and KNOX1 activity correlate with the evolution of a unifoliate body plan in Gesneriaceae Kanae Nishii1,2 & Bing-Hong Huang3 & Chun-Neng Wang4 & Michael Möller1 Received: 6 March 2016 /Accepted: 24 November 2016 /Published online: 8 December 2016 # Springer-Verlag Berlin Heidelberg 2016 Abstract Typical dicots possess equal-sized cotyledons and (Brassicales, rosids). In all examined Lamiales samples, un- leaf-bearing shoots topped withashootapicalmeristem like Arabidopsis, BM activity accompanied by STM expres- (SAM), the source of lateral organs, and where KNOX1 ho- sion was found in both cotyledons in early stages. Foliage meobox genes act as key regulators. New World Gesneriaceae leaves of Gesneriaceae and Jovellana also showed the corre- show typical cotyledons, whereas Old World Gesneriaceae lation of BM and STM expression. An extension of BM ac- show anisocotyly, the unequal post-germination growth of tivity was found following a phylogenetic trajectory towards cotyledons, and include unifoliate (one-leaf) plants. One-leaf one-leaf plants where it is active throughout the lifetime of the plants show an extremely reduced body plan: the adult above- macrocotyledon. Our results suggest that KNOX1 involve- ground photosynthetic tissue consisting of a single cotyledon, ment in early cotyledon expansion originated early on in the a macrocotyledon enlarged by the basal meristem (BM), but diversification of Lamiales and is proposed as the prerequisite lacking a SAM. To investigate the origin and evolution of the for the evolution of vegetative diversity in Gesneriaceae. Step- BM and one-leaf plants, the meristem activity and KNOX1 wise morphological shifts, driven by transfers of meristematic SHOOTMERISTEMLESS (STM) expression in cotyledons activity, as evidenced by shifts in KNOX1 expression, may be and leaves were systematically studied by RT-PCR and in situ one mechanism by which morphological diversity evolves in hybridization across the family Gesneriaceae, Jovellana in plants. Calceolariaceae (sister family to Gesneriaceae), and Antirrhinum in Plantaginaceae, all families of order Keywords KNOX1 . Streptocarpus . Gesneriaceae . Lamiales (asterids), in comparison to Arabidopsis Cotyledon . Leaf . Meristem Communicated by Sureshkumar Balasubramanian Introduction Electronic supplementary material The online version of this article (doi:10.1007/s00427-016-0568-x) contains supplementary material, Typical dicots possess equal-sized cotyledons and leaf- which is available to authorized users. bearing shoots topped with a shoot apical meristem (SAM), * Michael Möller though many variations exist. New World Gesneriaceae (sub- [email protected] family Gesnerioideae), in most cases, possess an above- ground morphology with a typical shoot system with the 1 Royal Botanic Garden Edinburgh, 20A Inverleith Row, SAM developing between two equal cotyledons (isocotyly) Edinburgh, Scotland EH3 5LR, UK and produce an ‘ordinary’ shoot structure with decussate leaf 2 Tokyo Gakugei University, 4-1-1 Nukuikitamachi, Koganei, arrangement (Fig. 1). On the other hand, the seedling mor- Tokyo 184-8501, Japan phology in Old World Gesneriaceae (subfamily 3 National Taiwan Normal University, No. 88, Sec. 4, Ting Chow Didymocarpoideae) is distinct from that of New World Road, Taipei 11677, Taiwan Gesneriaceae, because of anisocotyly, their unequal-sized 4 National Taiwan University, No.1, Sec. 4, Roosevelt Road, post-germination development of the cotyledons (Burtt Taipei 10617, Taiwan 1963;Fig.1d–g). In addition, there are variable shoot systems 42 Dev Genes Evol (2017) 227:41–60 Dev Genes Evol (2017) 227:41–60 43 Fig. 1 Experimental material selected across the Lamiales in a 1975; Harrison et al. 2005; Mantegazza et al. 2007) and uni- phylogenetic context (see Stevens 2001 onwards; Weber et al. 2013).a foliate Streptocarpus or Monophyllaea species (e.g. Tsukaya Antirrhinum majus, Plantaginaceae. b Jovellana punctata, Calceolariaceae. c Corytoplectus speciosus, New World Gesneriaceae 1997; Imaichi et al. 2000; Nishii et al. 2004; Ayano et al. (isocotylous). d–g Old World Gesneriaceae (anisocotylous). d 2005). Only the caulescent S. glandulosissimus with typical Henckelia anachoreta. e Streptocarpus glandulosissimus, caulescent with shoots has been studied in detail, and an area at the proximal typical shoot apical meristem (SAM). f, g Acaulescent Streptocarpus end of the leaf with an extended meristematic activity was lacking a shoot and SAM (Jong and Burtt 1975). f Streptocarpus rexii, rosulate, forming leaves from the groove meristem arranged in an irreg- found, similar to the basal meristem in phyllomorphs of acau- ular rosette (Jong and Burtt 1975). g Streptocarpus wendlandii,unifoliate, lescent Streptocarpus species (Nishii et al. 2010). Nothing is retaining the macrocotyledon as sole foliar organ (Hilliard and Burtt known in this respect from New World Gesneriaceae that do 1971). Column 1 habit, column 2 schematic illustration of cotyledon/ not exhibit anisocotyly, and thus, the critical questions to ad- leaf shape, column 3 SEM micrographs of seedlings, column 4 images of foliage leaves and macrocotyledon of the unifoliate S. wendlandii, dress are when the basal meristem has evolved in the evolu- column 5 descriptions of materials, from left to right: M meristem type, tion of Gesneriaceae, and where, in the cotyledon or leaves, it L leaf arrangement and type, C cotyledon type, S systematic position of was first established. This is particularly interesting with view the study material: *New World subfamily Gesnerioideae, **Old World to the evolution of plant meristems leading to unifoliate one- subfamily Didymocarpoideae. co cotyledon, Mc macrocotyledon, mc microcotyledon leaf plants, whether it is caused by an evolutionarily rapid truncation of the shoot or represents a gradual transition in shoot morphology (Hilliard and Burtt 1971; Cronk and recognized in Old World Gesneriaceae. The majority show a Möller 1997; Möller and Cronk 2001). typical shoot system with decussate leaf arrangement, but To this end, we selected species representing growth forms some show leafy organs without a typical SAM. of major lineages across the phylogeny of Gesneriaceae In Old World Gesneriaceae, one cotyledon, the (Möller et al. 2009, 2011; Möller and Clark 2013; Fig. 1, macrocotyledon, continues to grow after germination to al- Online Resource 1) and determined the position of cell divi- most resemble a foliage leaf, while the other, the sion activity in the cotyledon and leaf. Furthermore, the ex- microcotyledon, withers away eventually (Fig. 2a, b). The pression of class 1 KNOX homeobox (KNOX1) genes was degree of the macrocotyledon growth is different between evaluated since it was shown in the previous studies that in evolutionary lineages of Old World Gesneriaceae. In both cotyledons, leaves, and phyllomorphs of Streptocarpus, caulescent ones, such as Streptocarpus glandulosissimus,the KNOX1 has been found linked to the areas of meristematic anisocotyly phase, while short, delays the development of the activity (Mantegazza et al. 2009;Nishiietal.2010), and it is SAM but eventually forms a typical leaf-bearing shoot well established that KNOX1 genes function as regulators of (Fig. 2c). On the other hand, in acaulescent Streptocarpus, undifferentiated tissues and maintainers of meristematic prop- the macrocotyledon growth is greatly extended, sometimes erties in the SAM of angiosperms (Vollbrecht et al. 1991; for years, and they can reach >1 m in length, but no SAM is Smith et al. 1995;Longetal.1996), with formed (Fig. 2d, e; Jong 1970; Hilliard and Burtt 1971). Thus, SHOOTMERISTEMLESS (STM) being a major player in di- acaulescent Streptocarpus retain a ‘leafy organ’ originated cots (Long et al. 1996). Thus, we isolated STM homologues first from the macrocotyledon: the macrocotyledon enlarges from our study plants and determined their expression do- due to the activity of a basal meristem located at the proximal mains and employed them as the developmental genetic mark- end of the lamina and the petiolode meristem, a diffuse mer- er for meristem identity. To place the findings in a larger evo- istematic region of the petiole, near the base of the lamina, lutionary context, we compared the Gesneriaceae species to extending the petiole and midrib to form a leafy organ termed outgroup taxa across the core eudicots (i.e. asterids: Lamiales: ‘phyllomorph’, with the macrocotyledon forming the ‘cotyle- Jovellana punctata, Antirrhinum majus) including donary phyllomorph’ (Fig. 2d, e; Jong 1970; Jong and Burtt Arabidopsis thaliana (Brassicales, rosids; Online Resource 1). 1975). In rosulate acaulescent species, additional phyllomorphs are formed in an irregular arrangement from the groove meristem located on the adaxial side of the petiole Materials and methods near the base of the lamina (Figs. 1f and 2d). In unifoliate acaulescent species, no further phyllomorphs are formed, Plant materials and the cotyledonary phyllomorph is the only above-ground organ of the plant, producing inflorescences at the base of the Plant and seed materials were provided by the Royal Botanic lamina (Figs. 1g and 2e; Jong 1970; Jong and Burtt 1975; Garden Edinburgh (RBGE), Taipei Botanic Garden (Taiwan), Imaichi et al. 2000). and Cecilia Koo Conservation Center (Taiwan). Seeds of some The leaf ontogeny in Gesneriaceae has previously been outgroup species