Microanatomy of the placenta of Lycopodium obscurum: novel design in an underground embryo
2013
Renzaglia, Karen S. | Whittier, Dean P.
Background and Aims Long-lived underground populations of mycoheterotrophic gametophytes and attached sporophytes at various developmental stages occur in lycophytes. Young underground sporophytes obtain carbon solely from the gametophyte and establish nutritional independence only after reaching the soil surface, which may take several years. This prolonged period of matrotrophy exceeds that of bryophytes. The foot is massive and provides the lifeline for sporophyte establishment, yet the fine structure of the placental region is unexplored in lycophytes with underground gametophytes. Methods Gametophytes with attached embryos/young sporophytes of Lycopodium obscurum were collected in nature, processed and examined by light and transmission electron microscopy. Key Results Three ultrastructurally distinct regions were identified within a single foot of a sporophyte emerging from the soil. Young foot regions actively divide, and have direct contact with and show little differentiation from gametophyte cells. In unlobed foot areas, cells in both generations exhibit polarity in content and indicate unidirectional transport of carbon reserves into the foot toward the developing shoot and root. The foot has inconspicuous wall ingrowths. Highly lobed foot regions contain peripheral transfer cells with prominent wall ingrowths that absorb nutrients from degenerating gametophyte cells. Conclusions Variability within a single placenta is consistent with an invasive and long-lived foot. The late appearance of wall ingrowths in transfer cells reflects this dynamic ever-growing embryo. Placental features in lycophytes are related to the unique reorientation of all embryonic regions during development. Small placentas with wall ingrowths in both generations characterize ephemeral embryos in green gametophytes, while short-lived and repositioning embryos of heterosporous taxa are devoid of transfer cells. Transfer cell evolution across embryophytes is riddled with homoplasy and reflects diverse patterns of embryology. Scrutiny of placental evolution must include consideration of nutritional status and life history strategies of the gametophyte and young sporophyte.
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