Proper activity of the age‐dependent <scp>miR156</scp> is required for leaf heteroblasty and extrafloral nectary development in <i>Passiflora</i> spp.
Passion flower extrafloral nectaries (EFNs) protrude from leaves and facilitate mutualistic interactions with insects; however, how age cues control EFN growth remains poorly understood. Here, we examined leaf and EFN morphology and development of two Passiflora species with distinct leaf shapes, and compared the phenotype of these to transgenics with manipulated activity of the age-dependent miR156, which targets several SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE (SPL) transcription factors. Low levels of miR156 correlated with leaf maturation and EFN formation in Passiflora edulis and P. cincinnata. Accordingly, manipulating miR156 activity affected leaf heteroblasty and EFN development. miR156-overexpressing leaves exhibited less abundant and tiny EFNs in both Passiflora species. EFN abundance remained mostly unchanged when miR156 activity was reduced, but it led to larger EFNs in P. cincinnata. Transcriptome analysis of young leaf primordia revealed that miR156-targeted SPLs may be required to properly express leaf and EFN-associated genes. Importantly, altered miR156 activity impacted sugar profiles of the nectar and modified ecological relationships between EFNs and ants. Our work provides evidence that the miR156/SPL module indirectly regulates EFN development in an age-dependent manner and that the EFN development program is closely associated with the heteroblastic developmental program of the EFN-bearing leaves.
Authors
- Lana Laene Lima Dias (ORCID: https://orcid.org/0000-0002-0776-6039)
- Yoan Camilo Guzmán Sarmiento (ORCID: https://orcid.org/0000-0002-2193-7199)
- Lázara Aline Simões Silva (ORCID: https://orcid.org/0000-0003-0450-1809)
- Valéria Monteze Guimarães (ORCID: https://orcid.org/0000-0002-0735-6144)
- Wagner Campos Otoni (ORCID: https://orcid.org/0000-0002-9614-9373)
- Jessica Soares (ORCID: https://orcid.org/0009-0007-1109-4494)
- Lílian da Silva Fialho (ORCID: https://orcid.org/0000-0002-3722-2905)
- Elisandra da Silva Sousa (ORCID: https://orcid.org/0000-0002-4880-8389)
- Kerly Jessenia Moncaleano Robledo (ORCID: https://orcid.org/0000-0001-6205-9196)
- Flaviani Gabriela Pierdoná (ORCID: https://orcid.org/0000-0002-0755-5602)
- Jim P. Fouracre (ORCID: https://orcid.org/0000-0003-0049-3047)
- Claudinei da Silva Souza (ORCID: https://orcid.org/0000-0001-6701-9193)
- Elyabe Monteiro de Matos (ORCID: https://orcid.org/0000-0002-3466-4927)
- Fábio Tebaldi Silveira Nogueira (ORCID: https://orcid.org/0000-0001-6613-4069)
- Elisson Romanel (ORCID: https://orcid.org/0000-0002-4794-4215)
- Emerson Da Silveira (ORCID: https://orcid.org/0000-0002-7086-8492)
- Lyderson Fácio Viccini (ORCID: https://orcid.org/0000-0002-7575-8241)
- Pedro Alexandre Sodrzeieski (ORCID: https://orcid.org/0000-0003-3087-9362)
- Thaís Castilho de Arruda Falcão (ORCID: https://orcid.org/0009-0003-0469-0766)
- Vinícius Carius de Souza (ORCID: https://orcid.org/0000-0001-8075-3253)
Institutions
- Universidade Federal de Juiz de Fora (BR)
- Universidade Federal de Viçosa (BR)
- Universidade de São Paulo (BR)
- Instituto Butantan (BR)
- Museum and Institute of Zoology (PL)
- University of Bristol (GB)
- Polish Academy of Sciences (PL)
Publication Details
- Journal
- New Phytologist
- Published
- 2024-12-12
- DOI
- https://doi.org/10.1111/nph.20343
- Citations
- 4
- Primary Topic
- Plant Molecular Biology Research
- Type
- article
- Field-Weighted Citation Impact
- 2.40
Funders
- Fundação de Amparo à Pesquisa do Estado de São Paulo
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Fundação de Amparo à Pesquisa do Estado de Minas Gerais