Beyond pollination: diversity of secretory structures during flower development in different legume lineages

Barros, Thais Cury De; Marinho, Cristina Ribeiro; Pedersoli, Giseli Donizete; Paulino, Juliana Vilella; Teixeira, Simone Pádua

doi:10.1590/0102-33062016abb0291

ABSTRACT

Floral secretory structures are usually associated with the attraction of pollinators, but may also play an important role in the mechanisms of plant protection. This study aimed to show the diversity of secretory structures present in the developing flowers of 15 legume species belonging to different clades and to associate them with functions other than the pollinator attraction. Buds, flowers and developing axis of inflorescence were processed for surface, histological, and ultrastructural analyses. The species investigated displayed a wide diversity of secretory structures in developing flowers such as phenolic cells and/or tissues, mucilaginous cells, secretory cavities, secretory trichomes and colleters. Each type of secretory structure exhibited variation in morphology and location in the flower and/or axis of inflorescence depending on the species. Special mucilage cells, secretory cavities, secretory trichomes and colleters have great potential for comparative morphological studies due to their diversity of forms or restricted occurrence to certain taxa, contributing to a more robust morphological data base for the new clades emerging in Leguminosae. The scarcity of reports about floral secretory structures of Leguminosae seems to be more related to deficient sampling than to the absence of such structures in the group, which highlights the need for further investigation.

Keywords:
anatomy; colleter; Fabaceae; gland; idioblast; Leguminosae; morphology; mucilage cells; secretory cavity; secretory trichome

[1] * Corresponding author: spadua@fcfrp.usp.br

Clade	Species	Collection site	Natural habitat	Voucher	Herbarium
Cassia clade	Cassia fistula L.	Ribeirão Preto, SP (campus da USP)	Tropical and subtropical forest	JV Paulino 13	SPFR
Caesalpinia clade	Caesalpinia echinata Lam.	Ribeirão Preto, SP (campus da USP)	Atlantic Rainforest	SP Teixeira 67	SPFR
Dimorphandra p.p. clade	Dimorphandra mollis Benth.	São Carlos, SP (original vegetation)	Brazilian savanna	TC Barros 20	SPFR
Detarieae clade	Hymenaea courbaril L.	Ribeirão Preto, SP (campus da USP)	Brazilian savanna	SP Teixeira 45	SPFR
Mimosoideae clade	Calliandra brevipes Benth.	Ribeirão Preto, SP (campus da USP)	Amazonian Rainforest, Caatinga, Brazilian savanna, Atlantic Rainforest, Pampas	SP Teixeira 77	SPFR
Mimosoideae clade	Inga bella M. Sousa	Costa Rica (original vegetation)	Tropical forest	R Aguilar 12746	SPFR
Mimosoideae clade	Mimosa lewisii Barneby	Morro do Chapéu, BA (original vegetation)	Caatinga	SP Teixeira 76	SPFR
Mimosoideae clade	Tetrapleura tetraptera (Schumach. & Thonn.) Taub.	Jardim Botânico do Rio de Janeiro, RJ (cultivated)	West African Rainforest	TC Barros 05	SPFR
Papilionoideae clade	Erythrina speciosa Andrews	Ribeirão Preto, SP (campus da USP)	Brazilian savanna, Atlantic Rainforest	TC Barros 33	SPFR
Papilionoideae clade	Gliricidia sepium (Jacq.) Kunth ex Walp.	Ribeirão Preto, SP (campus da USP)	Amazonian Rainforest, Caatinga, Brazilian savanna, Atlantic Rainforest	SP Teixeira 62	SPFR
Papilionoideae clade	Indigofera lespedezioides Kunth	Ribeirão Preto, SP (campus da USP)	Amazonian Rainforest, Brazilian savanna, Atlantic Rainforest	MS Ogasawara 9926	SPFR
Papilionoideae clade	Leptolobium elegans Vogel	Campinas, SP	Amazonian Rainforest, Brazilian savanna	RS Rodrigues & A Flores 993	UEC
Papilionoideae clade	Mucuna urens (L.) Medik.	BR 101 km 11-13 (original vegetation)	Atlantic Rainforest	SP Teixeira 58	SPFR
Papilionoideae clade	Platycyamus regnellii Benth.	Ribeirão Preto, SP (campus da USP)	Brazilian savanna, Atlantic Rainforest	SP Teixeira 54	SPFR
Papilionoideae clade	Tipuana tipu (Benth.) Kuntze	Ribeirão Preto, SP (campus da USP)	Brazilian savanna, Atlantic Rainforest	SP Teixeira 51	SPFR

Traditional subfamily	Clade	Species	Secretory structures	Location	Morphology of the secretory structures
Caesalpinioideae	Cassia clade	Cassia fistula	Secretory trichomes	Axis of the inflorescence, base of the floral receptacle and the margins of bracts and bracteoles	Grouped multicellular trichomes with no apparent distinction between peduncle and head - colleter (Fig. 6A, C)
Caesalpinioideae	Caesalpinia clade	Caesalpinia echinata	Phenolic cells and tissues	Phenolic idioblasts in the mesophyll of bracts, sepals and petals Phenolic epidermis in the sepals	Voluminous idioblasts with the vacuole filled with phenolic compounds occupying the entire cell volume (Fig. 2C) Phenolic epidermis consistting of less voluminous cells than idioblasts, with the vacuole filled with phenolic compounds occupying the entire cell volume (Fig. 2C)
Caesalpinioideae	Dimorphandra p.p. clade	Dimorphandra mollis	Mucilaginous epidermis	Bract and sepals	Voluminous cells with thick walls largely consisting of mucilage and a distinct cytoplasm (Fig. 3A, B)
			Phenolic cells and tissues	Phenolic cells grouped in the subepidermal layers (cortex) of the axis of inflorescence Phenolic epidermis of petals and carpel Phenolic parenchyma (mesophyll) of bracts, sepals, petals and carpel	The phenolic cells of the axis of the inflorescence, bract, sepals and carpel are voluminous and their vacuoles are filled with phenolic compounds occupying the entire cell volume (Figs. 2E, 3A) Cells of the petal parenchyma and epidermis and of the carpel are more isodiametric and have a smaller vacuole (Figs. 2E, 3A)
			Secretory trichomes	Axis of the inflorescence	Usually grouped with a multicellular and multiseriate peduncle narrower than the multicellular secretory head consisting of voluminous cells; presence of phenolic compounds in the cells of the peduncle.
Caesalpinioideae	Detarieae clade	Hymenaea courbaril	Secretory cavities	Mesophyll of sepals and petals	Secretory cavities with epithelium consisting of a layer of secretory cells delimiting a lumen (Fig. 4A-D).
Caesalpinioideae	Detarieae clade	Hymenaea courbaril	Phenolic cells and tissues	Phenolic epidermis of sepals and petals Phenolic parenchyma of sepals and petals	The phenolic cells of the epidermis are more rectangular and smaller than the phenolic cells of the parenchyma (Fig. 3A-D) The phenolic cells of the parenchyma of sepals and petals have a vacuole filled with phenolic compounds and are more voluminous when located close to the secretory cavities (Fig. 3A-D)
Mimosoideae	Mimosoideae clade	Calliandra brevipes	Phenolic cells and tissues	Phenolic cells grouped in the subepidermal layers of the abaxial surface of bract, sepals and petals Phenolic parenchyma of the cortex and medulla of the axis of the inflorescence	Voluminous phenolic cells with a vacuole filled with phenolic compounds in the subepidermal layers of the abaxial surface of bract, sepals and petals (Fig. 2D) Phenolic epidermis consisting of rectangular cells smaller than the cells of the subepidermal layers Parenchymal cells with a vacuole filled with phenolic compounds, more voluminous in the medulla than in the cortex (Fig. 2F)
Mimosoideae	Mimosoideae clade	Calliandra brevipes	Secretory trichomes	Axis of the inflorescence, bract, margins of sepals and petals	Trichomes with a multicellular and uniseriate peduncle narrower than the multicellular secretory head with more voluminous cells; phenolic compounds present in the vacuole of cells of the peduncle and head (Fig. 4A, B)
Mimosoideae	Mimosoideae clade	Inga bella	Secretory trichomes	Margins of bract and sepals	Trichomes with a multicellular and uniseriate peduncle narrower than the secretory head, which is also multicellular (Fig. 5C, D)
Mimosoideae	Mimosoideae clade	Mimosa lewisii	Mucilaginous epidermis	Sepal	Voluminous cells with thick walls largely consisting of mucilage and a distinct cytoplasm (Fig. 3C-F)
			Phenolic cells and tissues	Phenolic cells in the mesophyll of the axis of the inflorescence, bract, sepal and carpel Phenolic epidermis of the sepals	Voluminous phenolic idioblasts with a vacuole filled with sparse phenolic compounds in the mesophyll of the sepal (Fig. 3D) Phenolic cells grouped in the subepidermal layers of the bract Phenolic epidermis on the abaxial surface of the sepal consisting of voluminous cells with a vacuole filled with phenolic compounds (Fig. 3E, F)
			Secretory trichomes	Axis of the inflorescence and bract	Large secretory trichomes with a robust peduncle and a small head; peduncle with accumulation of phenolic compounds (Fig. 5E, F) Secretory trichomes of phenolic compounds, with no apparent distinction between peduncle and head - colleter (Fig. 6F)
Mimosoideae	Mimosoideae clade	Tetrapleura tetraptera	Secretory trichomes	Base of the flower bud	Trichomes with a multicellular and multiseriate peduncle narrower than the multicellular secretory head and with more voluminous cells; phenolic compounds present in the vacuoles of the cells of the peduncle (Fig. 5G, H)
Papilionoideae	Papilionoideae clade	Leptolobium elegans	Secretory trichomes	Axilla of the bracts, bracteoles and axis of the inflorescence	Grouped multicellular trichomes with no apparent distinction between peduncle and head - colleter (Fig. 6B)
Papilionoideae	Papilionoideae clade	Erythrina speciosa	Phenolic cells	Mesophyll of the sepals and stamen filament	Sparse and non-voluminous idioblasts close to the vascular bundles
Papilionoideae	Papilionoideae clade	Erythrina speciosa	Secretory trichomes	Sepals	Trichomes with a multicellular and uniseriate peduncle with no apparent distinction from the more voluminous multicellular secretory head
Papilionoideae	Papilionoideae clade	Gliricidia sepium	Phenolic cells	Mesophyll of the axis of the inflorescence, sepals and carpel	Sparse and very voluminous idioblasts with a vacuole filled with phenolic compounds occupying the entire cell volume (Fig. 2B)
Papilionoideae	Papilionoideae clade	Gliricidia sepium	Secretory trichomes	Axis of the inflorescence, base of the flower bud	Multicellular trichomes with no apparent distinction between peduncle and head - colleter (Fig. 6E)
Papilionoideae	Papilionoideae clade	Indigofera lespedezioides	Secretory trichomes	Axilla of the bracts, bracteoles and axis of the inflorescence	Grouped multicellular trichomes with no apparent distinction between peduncle and head - colleter
Papilionoideae	Papilionoideae clade	Mucuna urens	Phenolic cells	Mesophyll of the sepals and stamen filament	Non-voluminous phenolic idioblasts close to the vascular bundles
Papilionoideae	Papilionoideae clade	Mucuna urens	Secretory trichomes	Base of the flower bud and sepals	Trichomes with a multicellular and uniseriate peduncle narrower than the multicellular head
Papilionoideae	Papilionoideae clade	Platycyamus regnellii	Phenolic cells	Mesophyll of the sepals, stamen filament and carpel	Non-voluminous phenolic idioblasts close to the vascular bundles
	Papilionoideae clade	Platycyamus regnellii	Secretory trichomes	Bract, sepals and carpel	Trichomes with a multicellular and uniseriate peduncle narrower than the multicellular head - colleter (Fig. 6D)
	Papilionoideae clade	Tipuana tipu	Phenolic cells	Mesophyll of the sepals, petals, filament thread and carpel wall	Sparse and very voluminous idioblasts with the vacuole filled with phenolic compounds occupying the entire cell volume and concentrated close to the vascular bundles or in the subepidermal layers of the sepals (Fig. 2A)

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Beyond pollination: diversity of secretory structures during flower development in different legume lineages

ABSTRACT