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Growth form evolution in Piperales and its relevance for understanding angiosperm diversification: an integrative approach combining plant architecture, anatomy and biomechanics

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Abstract
A striking feature of early angiosperm lineages is the variety of life forms and growth forms, which ranges from herbs, aquatic herbs, climbers, and epiphytes to woody shrubs and trees. This morphological and anatomical diversity is arguably one of the factors explaining how angiosperms dominate many ecosystems worldwide. However, just how such a wide spectrum of growth forms has evolved in angiosperms remains unclear. In this review, we investigate patterns of growth form diversification in Piperales, an early-diverging lineage (with stem age estimated at 201-128 Myr ago) and the most morphologically diverse clade among magnoliids. We outline patterns of growth form diversity and architecture as well as the biomechanical significance of developmental characters, such the organization, loss, and gain of woodiness. Asaroideae and Saururaceae are terrestrial as well as semiaquatic to aquatic herbaceous perennials bearing rhizomes. The Aristolochioideae and Piperaceae show higher levels of growth form diversity and biomechanical organization, with complex patterns of increasing or decreasing woodiness and architectural organization. The climbing habit has probably evolved independently in the Aristolochiaceae and Piperaceae, while mechanically unstable shrubs and, less frequently, treelets have evolved several times within these two most species-rich clades. A key developmental character underlying diversity in most Piperales-with the exception of the herbaceous Saruma (Asaroideae)-is the conserved development of the wood cylinder, in which fusiform initials are limited to fascicular carnbial initials. The resulting large fraction of raylike tissue in the stem-a highly characteristic feature of woody species in the Piperales-potentially introduced mechanical constraints on the diversification of self-supporting architectures. This was possibly circumvented by the architectural development of repeated, large-diameter meristems in some shrublike habits via sympodial growth. Patterns of growth form evolution within Piperales potentially mirror some of the overall trends observed among early-diverging angiosperms as a whole as well as angiosperms in general. These include profound changes in life form and growth form linked to large-scale transitions in woodiness, diversity of mechanical organization, and shifts in architectural development.
Keywords
anatomy, architecture, LAND PLANTS, LEAF ANATOMY, VESSEL EVOLUTION, SECONDARY GROWTH, TRACHEID MICROSTRUCTURE, THOTTEA ARISTOLOCHIACEAE, PHYLOGENETIC-RELATIONSHIPS, PEPEROMIA PIPERACEAE, SARUMA-HENRYI OLIV, SUBGENUS TILDENIA PIPERACEAE, Piperales, growth form, biomechanics, evolution

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Chicago
Isnard, Sandrine, Juliana Prosperi, Stefan Wanke, Sarah T Wagner, Marie-Stéphanie Samain, Santiago Trueba, Lena Frenzke, Christoph Neinhuis, and Nick P Rowe. 2012. “Growth Form Evolution in Piperales and Its Relevance for Understanding Angiosperm Diversification: An Integrative Approach Combining Plant Architecture, Anatomy and Biomechanics.” International Journal of Plant Sciences 173 (6): 610–639.
APA
Isnard, S., Prosperi, J., Wanke, S., Wagner, S. T., Samain, M.-S., Trueba, S., Frenzke, L., et al. (2012). Growth form evolution in Piperales and its relevance for understanding angiosperm diversification: an integrative approach combining plant architecture, anatomy and biomechanics. INTERNATIONAL JOURNAL OF PLANT SCIENCES, 173(6), 610–639.
Vancouver
1.
Isnard S, Prosperi J, Wanke S, Wagner ST, Samain M-S, Trueba S, et al. Growth form evolution in Piperales and its relevance for understanding angiosperm diversification: an integrative approach combining plant architecture, anatomy and biomechanics. INTERNATIONAL JOURNAL OF PLANT SCIENCES. 2012;173(6):610–39.
MLA
Isnard, Sandrine, Juliana Prosperi, Stefan Wanke, et al. “Growth Form Evolution in Piperales and Its Relevance for Understanding Angiosperm Diversification: An Integrative Approach Combining Plant Architecture, Anatomy and Biomechanics.” INTERNATIONAL JOURNAL OF PLANT SCIENCES 173.6 (2012): 610–639. Print.
@article{3028428,
  abstract     = {A striking feature of early angiosperm lineages is the variety of life forms and growth forms, which ranges from herbs, aquatic herbs, climbers, and epiphytes to woody shrubs and trees. This morphological and anatomical diversity is arguably one of the factors explaining how angiosperms dominate many ecosystems worldwide. However, just how such a wide spectrum of growth forms has evolved in angiosperms remains unclear. In this review, we investigate patterns of growth form diversification in Piperales, an early-diverging lineage (with stem age estimated at 201-128 Myr ago) and the most morphologically diverse clade among magnoliids. We outline patterns of growth form diversity and architecture as well as the biomechanical significance of developmental characters, such the organization, loss, and gain of woodiness. Asaroideae and Saururaceae are terrestrial as well as semiaquatic to aquatic herbaceous perennials bearing rhizomes. The Aristolochioideae and Piperaceae show higher levels of growth form diversity and biomechanical organization, with complex patterns of increasing or decreasing woodiness and architectural organization. The climbing habit has probably evolved independently in the Aristolochiaceae and Piperaceae, while mechanically unstable shrubs and, less frequently, treelets have evolved several times within these two most species-rich clades. A key developmental character underlying diversity in most Piperales-with the exception of the herbaceous Saruma (Asaroideae)-is the conserved development of the wood cylinder, in which fusiform initials are limited to fascicular carnbial initials. The resulting large fraction of raylike tissue in the stem-a highly characteristic feature of woody species in the Piperales-potentially introduced mechanical constraints on the diversification of self-supporting architectures. This was possibly circumvented by the architectural development of repeated, large-diameter meristems in some shrublike habits via sympodial growth. Patterns of growth form evolution within Piperales potentially mirror some of the overall trends observed among early-diverging angiosperms as a whole as well as angiosperms in general. These include profound changes in life form and growth form linked to large-scale transitions in woodiness, diversity of mechanical organization, and shifts in architectural development.},
  author       = {Isnard, Sandrine and Prosperi, Juliana and Wanke, Stefan and Wagner, Sarah T and Samain, Marie-St{\'e}phanie and Trueba, Santiago and Frenzke, Lena and Neinhuis, Christoph and Rowe, Nick P},
  issn         = {1058-5893},
  journal      = {INTERNATIONAL JOURNAL OF PLANT SCIENCES},
  keyword      = {anatomy,architecture,LAND PLANTS,LEAF ANATOMY,VESSEL EVOLUTION,SECONDARY GROWTH,TRACHEID MICROSTRUCTURE,THOTTEA ARISTOLOCHIACEAE,PHYLOGENETIC-RELATIONSHIPS,PEPEROMIA PIPERACEAE,SARUMA-HENRYI OLIV,SUBGENUS TILDENIA PIPERACEAE,Piperales,growth form,biomechanics,evolution},
  language     = {eng},
  number       = {6},
  pages        = {610--639},
  title        = {Growth form evolution in Piperales and its relevance for understanding angiosperm diversification: an integrative approach combining plant architecture, anatomy and biomechanics},
  url          = {http://dx.doi.org/10.1086/665821},
  volume       = {173},
  year         = {2012},
}

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