Entry and colonization of Asparagus officinalis roots by arbuscular mycorrhizal fungi with emphasis on changes in host microtubules

First-order lateral roots of Asparagus officinalis L. have a dimorphic exodermis consisting of short and long cells. Short cells have a thickened outer tangential wall, retain their cytoplasm, appear to have high levels of Ca2+, and undergo suberization later than contiguous long cells. In regions of the root in which the dimorphic nature of the exodermis is clearly evident, short cells have numerous cortical microtubules arranged predominantly in the transverse plane in reference to the long axis of the root. Arbuscular mycorrhizal fungi (either indigenous unidentified species in field-grown plants or Glomus intraradices Schenck & Smith in colonized plants in a growth chamber) form appressoria on epidermal cells located above exodermal short cells and infection hyphae then penetrate the outer tangential wall of short cells. A hyphal coil forms in short cells, and microtubules become closely associated with the coil; some cortical microtubules are retained in colonized short cells. A typical Arum type of arbuscular mycorrhizal association forms in the cortex, and concomitant with this, a rearrangement of microtubules occurs. During arbuscule formation, microtubules are associated with the large trunk hypha and with the fine arbuscule branches; cortical microtubules, although reduced in number, are present. As the arbuscule degenerates, a few microtubules are still associated with the hyphal clump and many cortical microtubules, oriented primarily in a transverse plane, are present. This study shows that arbuscular mycorrhizal fungi interact closely with the microtubular component of the cytoskeleton from the earliest stages of entry through arbuscule degeneration. These results support the concept that biotrophic fungal species have evolved intimate associations with plant cells.