The preprophase band of microtubules controls the robustness of division orientation in plants

Abstract

Controlling cell division plane orientation is essential for morphogenesis in multicellular organisms. In plant cells, the future cortical division plane is marked before mitotic entry by the preprophase band (PPB). Here, we characterized an (TON1 Recruiting Motif) mutant that impairs PPB formation but does not affect interphase microtubules. Unexpectedly, PPB disruption neither abolished the capacity of root cells to define a cortical division zone nor induced aberrant cell division patterns but rather caused a loss of precision in cell division orientation. Our results advocate for a reassessment of PPB function and division plane determination in plants and show that a main output of this microtubule array is to limit spindle rotations in order to increase the robustness of cell division.

Division Plane Orientation Defects Revealed by a Synthetic Double Mutant Phenotype

“…Many mutants with cells that never formed PPBs also have significant defects in cortical microtubule organization and cell expansion, making it difficult to separate the interphase function from the G2 or mitotic function (Camilleri et al, 2002;Azimzadeh et al, 2008;Wright et al, 2009;Spinner et al, 2010Spinner et al, , 2013Kirik et al, 2012). Two interesting exceptions of mutants lacking obvious PPBs have recently been identified: tonneau1a (Zhang et al, 2016) and a triple mutant in three related trm loci (Schaefer et al, 2017). One hypothesis is that the mostly normal cortical microtubule array without a PPB is sufficient to direct the formation of a properly placed new cell wall.…”

“…Although the location of the PPB accurately predicts the future division site (Gunning et al, 1978;Van Damme et al, 2007;Rasmussen et al, 2013;Lipka et al, 2014;Martinez et al, 2017), its role in division plane establishment has recently been called into question by mutants that do not form obvious PPBs but manage to produce relatively orderly roots. These plants have mutations in the tonneau1a locus (Zhang et al, 2016) and mutations in three related tonneau1 recruiting motif (trm) loci (Schaefer et al, 2017). Whether the PPB establishes the future division site or is the signpost of an earlier established cue for the future division site remains an active area of investigation.…”

“…Whether the PPB establishes the future division site or is the signpost of an earlier established cue for the future division site remains an active area of investigation. The PPB is a transient structure that forms in G2 and promotes proper spindle orientation (Chan et al, 2005;Ambrose and Cyr, 2008;Schaefer et al, 2017) but then disappears from the cortex. The PPB is thought to leave behind a division site marker that recruits the division machinery to the correct location (Rasmussen et al, 2013).…”

Cytoplasmic MTOCs control spindle orientation for asymmetric cell division in plants

“…For instance, without centrosomes or the PPB, the chloronemal apical cells of moss invariably orient the spindle along the cell's long axis and the division plane perpendicular to it (15,16). Moreover, the recently reported trm678 mutant that does not form obvious PPBs only causes some loss of precision in division plane orientation and develops remarkably normally (17). Overall, the mechanism of division axis determination is still not well understood in plants.…”

The Role of the Primary Cell Wall in Plant Morphogenesis

“…Stress also predicts the plane of cell division marked by the preprophase band of microtubules [80] as putative mitosis stabilisers [81] and the appearance of the cell plate templated by extensin self-assembling amphiphiles; [82] hydroxyproline-rich glycoproteins central to plant growth, once again cooperate with biomechanical forces. Elegant laser ablation experiments alter the orientation of PIN proteins in the apical meristem [26].…”