Background <p>Petals are a key evolutionary innovation of flowers that reshape plant-pollinator interactions and contribute to the dominance of angiosperms in terrestrial ecosystems. However, their evolutionary origin remains debated as previous studies have largely relied on morphological inferences with limited spatially resolved molecular evidence during floral organogenesis.</p> Results <p>Here we employ spatial transcriptome sequencing on developing floral buds of the basal angiosperm <i>Nymphaea colorata</i> to dissect the potential gene regulatory landscape underlying petal formation. Our analyses reveal an unexpected hierarchical structure of four meristematic cell groups that persist at the floral base until carpel formation, displaying a gradient of decreasing meristematic potential along the proximal–distal axis. Among them, one group gives rise to stamens and petals (inner tepals). Developmental trajectory reconstruction further uncovers successive cell-fate transitions from stamen primordium to developing petals. These transitions are driven by quantitative variation in MADS-box tetramers composition that gradually reduces the reproductive identity of outer-whorl floral organs. Spatial mapping of developmental regulatory modules involving thousands of tissue-preferentially expressed genes demonstrate that petal morphogenesis integrates additional leaf-like genetic programs, ultimately distinguishing petals from stamens.</p> Conclusions <p>Together, these results uncover the evolutionary derivation of petals from reproductive organs through recruitment of ancestral regulatory networks established before seed plants, providing new insights into the developmental basis and evolutionary innovation of petaloid organs in flowering plants.</p>

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Spatiotemporal transcriptome atlas of water lily floral organogenesis provides insight to the evolutionary origin of petals in basal angiosperms

  • Chang Liu,
  • Ge Wang,
  • Binbin Cao,
  • Yonglong Li,
  • Yamao Chen,
  • Chunce Guo,
  • Ji Qi

摘要

Background

Petals are a key evolutionary innovation of flowers that reshape plant-pollinator interactions and contribute to the dominance of angiosperms in terrestrial ecosystems. However, their evolutionary origin remains debated as previous studies have largely relied on morphological inferences with limited spatially resolved molecular evidence during floral organogenesis.

Results

Here we employ spatial transcriptome sequencing on developing floral buds of the basal angiosperm Nymphaea colorata to dissect the potential gene regulatory landscape underlying petal formation. Our analyses reveal an unexpected hierarchical structure of four meristematic cell groups that persist at the floral base until carpel formation, displaying a gradient of decreasing meristematic potential along the proximal–distal axis. Among them, one group gives rise to stamens and petals (inner tepals). Developmental trajectory reconstruction further uncovers successive cell-fate transitions from stamen primordium to developing petals. These transitions are driven by quantitative variation in MADS-box tetramers composition that gradually reduces the reproductive identity of outer-whorl floral organs. Spatial mapping of developmental regulatory modules involving thousands of tissue-preferentially expressed genes demonstrate that petal morphogenesis integrates additional leaf-like genetic programs, ultimately distinguishing petals from stamens.

Conclusions

Together, these results uncover the evolutionary derivation of petals from reproductive organs through recruitment of ancestral regulatory networks established before seed plants, providing new insights into the developmental basis and evolutionary innovation of petaloid organs in flowering plants.