Development and Fine Structure of the Glandular Trichomes of Artemisia annua L.

Abstract

Development of capitate glands on the leaves of annual wormwood (Artemisia annua L.) was monitored with scanning and transmission electron microscopy. Differentiation of foliar cells into gland cells began in the youngest leaf primordia. After differentiation into a 10-celled biseriate structure of two stalk cells, two basal cells, and three pairs of secretory cells, the cuticle of the six secretory cells separated from the cell walls to form a bilobed sac that eventually splits to release its contents. At every developmental stage, the cells of the the gland contained relatively little vacuolar volume. The secretory cells contained extensive endoplasmic reticulum. The plastids of each cell pair were different. At maturity, the apical cells contained proplastids or leucoplasts with only occasional thylakoids. The cell pair below the apical cell pair contained amorphous chloroplasts without starch grains. The basal cell pair contained proplastids or leucoplasts and the stalk cells contained chloroplasts. The stroma to thylakoid ratio in the secretory cell chloroplasts was high. Initially, osmiophilic product was observed most freqently associated with stacked thylakoids, plastid envelopes, and smooth endoplasmic reticulum, although it was associated with all cell membranes. Near the plasma membrane adjacent to cell walls bordering the subcuticular space, the cytoplasm was enriched in smooth endoplasmic reticulum containing osmiophilic material. The apical cell wall of the apical secretory cell pair was reticulated on the inner cytoplasmic side and contained osmiophilic staining on the cuticular side. During early senescence, osmiophilic product was commonly associated with outer mitochondrial membranes.

Bidirectional Secretions from Glandular Trichomes of Pyrethrum Enable Immunization of Seedlings

“…However, germacrene A synthase (germacrene A is a precursor of STLs in pyrethrum) has been only detected in chloroplast-free apical cells (Olofsson et al, 2012), and 1-deoxy-D-xylulose-5-phosphate reductoisomerase participating in the plastidial MEP pathway and linalool synthase were amplified only from the chloroplast-containing subapical cells (Olsson et al, 2009;Olofsson et al, 2012). A. annua trichomes have an additional stalk cell layer compared with pyrethrum glandular trichomes, but otherwise they are phenotypically very similar (Duke and Paul, 1993). Therefore, to understand the mechanism of selective secretion of STLs and pyrethrins, we propose that STLs of pyrethrum are mainly produced in the apical cell layer without chloroplasts, allowing immediate secretion into the subcuticular space, whereas monoterpenoid pyrethrin precursors are produced by the subapical cells with chloroplasts.…”

“…Secretion of pyrethrin precursors from these subapical cells may be blocked in the apical direction, resulting in default secretion in a basipetal direction, or, alternatively, there may be an active process involving specific proteins that transport monoterpenoid precursors of pyrethrins in the basipetal direction. Duke and Paul (1993) studied very similar glandular trichomes of A. annua and showed by transmission electron microscopy that osmiophilic (=lipid) material is produced profusely by chloroplast-containing subapical cells and is present between plasma membranes and cell walls that do not border the subcuticular space. This supports the contention that the subapical cells of biseriate capitate glandular trichomes from Asteraceae are able to secrete osmium-colored products (most likely terpenoids) into the intercellular space, even though it does not prove that basipetal transport occurs.…”

“…The terpenoids produced in biseriate capitate glandular trichomes are thus far known to be secreted toward the apical side, resulting in a droplet of secondary metabolites in an extracellular cavity covered by a thick cuticular membrane (Duke and Paul, 1993;Fahn, 2000;Kutchan, 2005). The secretion of metabolites in a basipetal direction, across the epidermis, has not been described.…”

Artemisia annua mutant impaired in artemisinin synthesis demonstrates importance of nonenzymatic conversion in terpenoid metabolism

“…The production of artemisinin occurs in specialized 10-cell biseriate glandular trichomes present on the leaves, stems, and inflorescences of Artemisia annua (1)(2)(3). Artemisinin is phytotoxic (4) and is believed to accumulate in the subapical extracellular cavity of glandular trichomes (2).…”

Utilização de estruturas secretoras na identificação dos gêneros de Asteraceae de uma vegetação de cerrado

“…O mesmo tipo de estrutura secretora pode estar presente em todos os órgãos da planta ou pode estar confinado a apenas um órgão (Solereder 1908, Fahn 1979; pode-se encontrar, ainda, diferentes tipos nas partes de um mesmo vegetal (Solereder 1908, Esau 1977, Fahn 1979. Para a folha, considerando-se as Asteraceae, as investigações realizadas relataram a presença de oito diferentes tipos de estruturas secretoras: ductos (Fueyo 1986, Castro 1987, Maksymowych & Ledbetter 1987, Ascensão & Pais 1988, Joseph et al 1988, Lersten & Curtis 1988, Meira 1991, Claro 1994, cavidades ,1990, Fueyo 1986, Monteiro 1986, 1989, Monteiro et al 1995, idioblastos (Castro 1987, Meira 1991, Claro 1994, laticíferos (Vertrees & Mahlberg 1978), hidatódios (Perrin 1971, Lersten & Curtis 1985, Castro 1987, Meira 1991, Claro 1994, nectários extraflorais (O'Dowd & Catchpole 1983), tricomas (Carlquist 1958, Kelsey & Shafizadeh 1980, Werker & Fahn 1981,1982, Ascensão & Pais 1982, Castro 1987, Meira 1991, Duke & Paul 1993, Claro 1994) e apên-dices glandulares (Carlquist 1959a, b); nestes trabal...…”