4.7 Article

Tracing the opposing assimilate and nutrient flows in live conifer needles

期刊

JOURNAL OF EXPERIMENTAL BOTANY
卷 74, 期 21, 页码 6677-6691

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OXFORD UNIV PRESS
DOI: 10.1093/jxb/erad334

关键词

3D imaging; assimilate flow; bundle sheath; conifer needle; endodermis; esculin; fluorescence microscopy; micro-X-ray CT; nutrient flow; phloem; Pinus; transmission electron microscopy; xylem

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This study investigates the transportation pathway of photoassimilates and nutrients in conifer needles and reveals the functional 3D structure of the transfusion tissue in the bundle sheath. The results highlight the crucial role of the bundle sheath in nutrient and assimilate exchange.
The vasculature along conifer needles is fundamentally different from that in angiosperm leaves as it contains a unique transfusion tissue inside the bundle sheath. In this study, we used specific tracers to identify the pathway of photoassimilates from mesophyll to phloem, and the opposing pathway of nutrients from xylem to mesophyll. For symplasmic transport we applied esculin to the tip of attached pine needles and followed its movement down the phloem. For apoplasmic transport we let detached needles take up a membrane-impermeable contrast agent and used micro-X-ray computed tomography to map critical water exchange interfaces and domain borders. Microscopy and segmentation of the X-ray data enabled us to render and quantify the functional 3D structure of the water-filled apoplasm and the complementary symplasmic domain. The transfusion tracheid system formed a sponge-like apoplasmic domain that was blocked at the bundle sheath. Transfusion parenchyma cell chains bridged this domain as tortuous symplasmic pathways with strong local anisotropy which, as evidenced by the accumulation of esculin, pointed to the phloem flanks as the preferred phloem-loading path. Simple estimates supported a pivotal role of the bundle sheath, showing that a bidirectional movement of nutrient ions and assimilates is feasible and emphasizing the role of the bundle sheath in nutrient and assimilate exchange. Whole-needle tracer experiments and live fluorescence and X-ray imaging reveal extension of the phloem and xylem by the unique transfusion tissue, and bidirectional transcellular flow of nutrients and assimilates across the bundle sheath.

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