A Novel Putative Microtubule-Associated Protein Is Involved in Arbuscule Development during Arbuscular Mycorrhiza Formation

Abstract

The formation of arbuscular mycorrhizal (AM) symbiosis requires plant root host cells to undergo major structural and functional reprogramming to house the highly branched AM fungal structure for the reciprocal exchange of nutrients. These morphological modifications are associated with cytoskeleton remodelling. However, molecular bases and the role of microtubules (MTs) and actin filament dynamics during AM formation are largely unknown. In this study, the tomato tsb (tomato similar to SB401) gene, belonging to a Solanaceae group of genes encoding MT-associated proteins (MAPs) for pollen development, was found to be highly expressed in root cells containing arbuscules. At earlier stages of mycorrhizal development, tsb overexpression enhanced the formation of highly developed and transcriptionally active arbuscules, while tsb silencing hampers the formation of mature arbuscules and represses arbuscule functionality. However, at later stages of mycorrhizal colonization, tsb overexpressing (OE) roots accumulate fully developed transcriptionally inactive arbuscules, suggesting that the collapse and turnover of arbuscules might be impaired by TSB accumulation. Imaging analysis of the MT cytoskeleton in cortex root cells OE tsb revealed that TSB is involved in MT bundling. Taken together, our results provide unprecedented insights into the role of novel MAP in MT rearrangements throughout the different stages of the arbuscule life cycle.

Microtubule cytoskeleton and mycorrhizal roots

“…To date, only a recent research has deepened into this question. 1 In this study, the authors identified the tomato Tsb gene induced in arbuscule-hosting cells and encoding a putative MAP. Their results pointed to a role of this protein for MT bundling and for proper arbuscule functionality.…”

“…The presence of a specific biological machinery commonly shared by arbuscule-containing cells and pollen tube cells has been suggested, 30 probably due to the fact that both cells types are subjected to strong polar modifications. Actually, transcriptomic comparisons performed in Medicago and tomato revealed significant overlaps between arbuscular mycorrhiza and pollen development, 1 , 30 with a predominance of genes related to the creation and modification of membranes and cell-walls. One of these overlapping genes is the tomato Tsb gene, which is specifically induced in pollen and in mycorrhizal roots.…”

“…It is believed that the cytoskeleton of the plant host plays an essential role in these processes, particularly the microtubule (MT) cytoskeleton, as huge modifications have been observed in the MT array of root cells accompanying the establishment of the AM symbiosis. Recent research 1 has established a link between microtubule rearrangements and arbuscule functioning. However, further research is required to elucidate the specific functions of MT cytoskeleton along the different stages of the arbuscule life cycle and to unravel the signals triggering these changes.…”

GR24, A Synthetic Strigolactone Analog, and Light Affect the Organization of Cortical Microtubules in Arabidopsis Hypocotyl Cells

“…, where I N = any given value of fluorescence intensity; I = the mean intensity value; N = the size of the dataset (i.e., the number of fluorescence intensity values); SD = the standard deviation [adapted from Higaki et al (2010)]. Skewness practically evaluates how much the fluorescence intensity of each given pixel in the image deviates from the mean value, or, in other words, how uniformly the sample is labeled.…”

“…Given the above information regarding the role of strigolactones and karrikins in plant morphogenetic processes, which are regulated in a hormone-dependent manner by cytoskeleton ( Blume et al, 2017 ), we studied herein the effects of strigolactone content modulators on microtubule organization and dynamics. Plant cytoskeleton is involved in many developmental processes regulated by plant hormones, e.g., the switch from cell division to cell expansion ( Ruan and Wasteneys, 2014 ), elongation and differentiation ( Ivakov and Persson, 2013 ; Ambrose and Wasteneys, 2014 ; Sampathkumar et al, 2014 ), in plant responses to salt ( Shoji et al, 2006 ) and osmotic stress ( Komis et al, 2002 ; Wang et al, 2010 ), as well as in the formation of arbuscular mycorrhiza ( Ho-Plágaro et al, 2021 ).…”