Control of patterns of symmetric cell division in the epidermal and cortical tissues of the Arabidopsis root

Abstract

Controlled cell division is central to the growth and development of all multicellular organisms. Within the proliferating zone of the Arabidopsis root, regular symmetric divisions give rise to patterns of parallel files of cells, the genetic basis of which remains unclear. We found that genotypes impaired in the TONNEAU1a (TON1a) gene display misoriented symmetric divisions in the epidermis and have no division defects in the underlying cortical tissue. The TON1a gene encodes a microtubule-associated protein. We show that in the ton1a mutant, epidermal and cortical cells do not form narrow, ring-like preprophase bands (PPBs), which are plant-specific, cytoskeletal structures that predict the position of the division plane before mitosis. The results indicate that in the cortex but not in the epidermis, division plane positioning and patterning can proceed correctly in the absence of both a functional TON1a and PPB formation. Differences between tissues in how they respond to the signals that guide symmetric division orientation during patterning might provide the basis for organised organ growth in the absence of cell movements.

Proper division plane orientation and mitotic progression together allow normal growth of maize

“…In addition, many symmetric division plane orientation mutants have defects in both interphase and mitotic microtubule dynamics, making it impossible to address mitotic and interphase function independently (10)(11)(12)(43)(44)(45)(46)(47). There are a few mutants that represent intriguing exceptions to highly pleiotropic mutants.…”

An overview of plant division‐plane orientation

“…These mutants display almost normal growth and mild division‐plane orientation defects (Zhang et al ., ; Schaefer et al ., ). The ton1a single mutant lacks proper PPBs, yet many divisions were still properly oriented, especially in root cortex cells (Zhang et al ., ). The triple trm 6,7,8 mutant lacks proper PPBs but grows well (Fig.…”

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.…”