TheMedicagoSpecies A2-Type Cyclin Is Auxin Regulated and Involved in Meristem Formation But Dispensable for Endoreduplication-Associated Developmental Programs

Abstract

(M.L., P.L., P.A.)Phytohormones as well as temporal and spatial regulation of the cell cycle play a key role in plant development. Here, we investigated the function and regulation of an alfalfa (Medicago sativa) A2-type cyclin in three distinct root developmental programs: in primary and secondary root development, nodule development, and nematode-elicited gall formation. Using transgenic plants carrying the Medsa;cycA2;2 promoter-␤-glucuronidase gene fusion, in combination with other techniques, cycA2;2 expression was localized in meristems and proliferating cells in the lateral root and nodule primordia. Rapid induction of cycA2;2 by Nod factors demonstrated that this gene is implicated in cell cycle activation of differentiated cells developing to nodule primordia. Surprisingly, cycA2;2 was repressed in the endoreduplicating, division-arrested cells both during nodule development and formation of giant cells in nematode-induced galls, indicating that CycA2;2 was dispensable for S-phase in endoreduplication cycles. Overexpression of cycA2;2 in transgenic plants corresponded to wild type protein levels and had no apparent phenotype. In contrast, antisense expression of cycA2;2 halted regeneration of somatic embryos, suggesting a role for CycA2;2 in the formation or activity of apical meristems. Expression of cycA2;2 was up-regulated by auxins, as expected from the presence of auxin response elements in the promoter. Moreover, auxin also affected the spatial expression pattern of this cyclin by shifting the cycA2;2 expression from the phloem to the xylem poles.Cyclins are the regulatory subunits of cyclindependent kinase complexes whose ordered, consecutive, and periodic activities drive the cell cycle. Cyclins are classified as G1 and mitotic cyclins. The latter group comprises the A-and B-type cyclins involved in the regulation of the cell cycle from the S to M phases. Cyclins are usually present for short periods in the cell cycle when they activate their CDK partners and determine the substrate specificity as well as the localization, maintenance and stability of these protein complexes. The activity of the cyclin-CDK complexes is tightly controlled during cell cycle and organ development.In plants, where organogenesis takes place continuously, most cells maintain their ability to re-enter and to regulate the cell cycle, in response to a wide range of external signals. The phytohormones, mostly auxin and cytokinin endogenously exert a temporal and local control on the cell cycle (Stals and Inzé, 2001). They act at multiple levels affecting transcription of cell cycle genes or the activity of the cyclin-dependent kinases; moreover, their altered balance seems to be required at specific points of the cell cycle. It is largely unknown how these external and internal signals interact and how their actions are coordinated and integrated into developmental programs.The plasticity of plant cell cycle may rely on the evolution of multiple cyclin forms. The sequence of the Arabidopsis genome indicates the existence ...

Root developmental programs shape theMedicago truncatulanodule meristem

“…As nodules are formed on roots it has been hypothesized that the nodule developmental program is derived from the lateral root developmental program (Nutman, 1948;Hirsch et al, 1997;Mathesius et al, 2000;de Billy et al, 2001;Roudier et al, 2003;Bright et al, 2005;Desbrosses and Stougaard, 2011). Recently, the expression of several root meristem regulators has been observed in the nodule meristem (NM) (Osipova et al, 2011(Osipova et al, , 2012Roux et al, 2014), thereby providing molecular support for this hypothesis.…”

Auxin acts as a local morphogenetic trigger to specify lateral root founder cells

“…Xylem pole pericycle cells, from which founder cells are recruited, carry cytological features such as dense cytoplasm, large nuclei, and small vacuoles typical of meristematic cells (13). In addition, it has been shown that these cells are capable of fast entry into the cell cycle because of sustained expression of cell cycle genes such as CDKA;1 or CycA2;1 (14,15). However, only very few cells of the pericycle tissue layer are recruited to become founder cells, and until now no founder cell-specific marker or mutants affected specifically in founder cell specification have been found (14).…”

Balance between cell division and differentiation during plant development

“…However, there is direct evidence that auxin also regulates the expression of some regulatory subunits. Thus, alfalfa CYCA2;2 expression is induced by auxin and during lateral root initiation and elongation (Roudier, et al, 2003). Consistent with such expression pattern, CYCA2 has been involved in mitotic cycles but not in endocycles and cell differentiation.…”