The transition from somatic to germline identity shows conserved and specialized features during angiosperm evolution

Abstract

How and why specific plant cells adopt germline identity during ovule development has proved challenging to address, and the pathways that are active in the ovules of basal/early-divergent angiosperms possessing a multilayered nucellus are still unclear. Here, we compare megasporogenesis between two early-divergent angiosperms (Annona cherimola and Persea americana) and the evolutionarily derived Arabidopsis thaliana, studying the three-dimensional spatial position of the megaspore mother cell (MMC), the compositional details of the MMC wall and the location of PIN1 expression. Specific wall polymers distinguished the central position of the MMC and its meiotic products from surrounding tissues in early-divergent angiosperms, whereas, in A. thaliana, only callose (in mature MMCs) and arabinogalactan proteins (AGPs) (in megaspores) distinguished the germline. However, PIN1 expression, which regulates polar auxin transport, was observed around the MMC in the single-layer nucellus of A. thaliana and in the multilayered nucellus of A. cherimola, or close to the MMC in P. americana. The data reveal a similar microenvironment in relation to auxin during megasporogenesis in all three species. However, the different wall polymers that mark MMC fate in early-divergent angiosperms may reflect a specific response to mechanical stress during differentiation, or the specific recruitment of polymers to sustain MMC growth.

Translating auxin responses into ovules, seeds and yield: Insight from Arabidopsis and the cereals

“…A similar pattern was observed for DR5:nlsGFP in young ovules from the daisy Hieracium piloselloides (Figure D, E; Tucker et al ), in early divergent angiosperms (Lora et al ) and in maize (Forestan and Varotto ; Lituiev et al ). In maize, DR5rev::mRFPer shows abundant expression in antipodal cells at the chalazal pole of the female gametophyte (Chettoor and Evans ).…”

“…Upon establishment of the primary germline cell (megaspore mother cell; MMC), expression of TAA1 is detected in the chalazal nucellus and inner integument primordia (Ceccato et al ; Robert et al ), which is complemented by expression of PIN1 and DR5 markers in the distal nucellar tissue (Pagnussat et al ; Bencivenga et al ). A similar pattern of PIN1 expression has been observed in cherimoya, avocado (Lora et al ) and maize (Forestan et al 2012). This pattern suggests that as ovule development proceeds, auxin is synthesized in the base and transported into the nucellar tissue surrounding the MMC, where it affects a response as the ovule progresses through meiosis and early (FG1 and FG2) stages of gametophyte development.…”

“…Reproductive expression (Marchant et al 1999) influx angiosperms (Lora et al 2017) and in maize (Forestan and Varotto 2012;Lituiev et al 2013). In maize, DR5rev:: mRFPer shows abundant expression in antipodal cells at the chalazal pole of the female gametophyte (Chettoor and Evans 2015).…”

The role of the integuments in pollen tube guidance in flowering plants

“…AGPs have also been observed in the micropylar nucellus of Amaranthus hypochondriacus (Coimbra & Salema, ) and in the micropyle and synergids of Arabidopsis thaliana (Coimbra et al ., ). Recent results have shown that cell wall polymers, including AGPs, mark the female germline in Annona cherimola , but not in Arabidopsis , and this could reflect the different microenvironment of nucellar cells around and during female germline development (Lora et al ., ). A different microenvironment is also found around the egg apparatus in the mature female gametophyte of Annona and Arabidopsis , and could also have implications for pollen tube guidance that have not yet been studied.…”

Pollen–pistil interaction in pawpaw (Asimina triloba), the northernmost species of the mainly tropical family Annonaceae

“…Indeed, the capacity of these sugary chains to detach from the cell wall and be secreted to the apoplast (Majewska‐Sawka and Nothnagel, 2000; Ellis et al, 2010) makes AGPs excellent candidates for cell–cell communication, critical during pollen–pistil interactions. During the reproductive process, AGPs have been associated with female gametogenesis (Acosta‐García and Vielle‐Calzada, 2004; Coimbra et al, 2007; Lopes et al, 2016; Lora et al, 2017), somatic embryogenesis (Pennell et al, 1992; van Hengel et al, 2002), pollen tube guidance toward the ovules (Mizukami et al, 2016), and pollen grain recognition (Pereira et al, 2015). Additionally, the secretion of AGPs correlates with the temporal window in which interactions between pollen tubes and the carpel tissues occur (Losada and Herrero, 2012, 2014, 2017; Pereira et al, 2015; Mizukami et al, 2016).…”