Mutations in the Arabidopsis RPK1 gene uncouple cotyledon anlagen and primordia by modulating epidermal cell shape and polarity

Abstract

SummaryPlant seedlings have either one or two cotyledons. The mechanisms that regulate this organ number are poorly understood. Mutations in the RECEPTOR-LIKE PROTEIN KINASE1 (RPK1) gene of the dicot Arabidopsis have only one cotyledon, with low penetrance due to complex genetic redundancy. An analysis of patterning genes required for cotyledon initiation showed that these have normal expression patterns, defining the cotyledon anlagen, in rpk1. This was also true for key genes, which organize the shoot apical meristem (SAM). By contrast, epidermal cell shape and polarity were compromised in rpk1 embryos, as evidenced by disturbed polarity of the auxin efflux carrier PIN1. PIN1 is required for the establishment of auxin maxima, which induce and maintain organ primordia. The effects in rpk1 mutants manifest in a spatially and timely stochastic fashion probably due to redundancy of RPK1-like functions. Consistently, auxin maxima showed a stochastic distribution in rpk1 embryos, being at times entirely absent and at other times supernumerary. This variability may explain how monocotyledonous seedlings and cotyledon shape variants can developmentally arise in Arabidopsis and possibly in other plants.

A Common Pathway of Root Growth Control and Response to CLE Peptides Through Two Receptor Kinases inArabidopsis

“…The auxin efflux carrier PIN-FORMED1 (PIN1) is not expressed in the defective half of the embryos lacking one cotyledon primordium, correlating with an absence of auxin maxima. A link between misregulated polarity of PIN1 in the epidermis of rpk1 and the occurrence of plants with one cotyledon was also recently demonstrated in the rpk1 embryos with cotyledon defects (Luichtl et al 2013).…”

Combining linkage and association mapping identifiesRECEPTOR-LIKE PROTEIN KINASE1as an essentialArabidopsisshoot regeneration gene

“…Importantly, single rpk1 mutants exhibit a recalcitrant shoot regeneration phenotype, and hence, in contrast to its role in embryogenesis, RPK1 plays an autonomous role in shoot organogenesis. Finally, several aspects described for RPK1 during embryo formation (36,46,48) support its involvement in regeneration: (i) RPK1 expression is important for PINFORMED1 localization, which is required for the establishment of auxin maxima, (ii) an RPK1-dependent pathway is thought to initiate WUS-RELATED HOMEOBOX5 expression, and (iii) RPK1 is assumed to receive intercellular signals and mediate intracellular responses required for pattern formation. Indeed, correct PINFORMED1 localization and auxin maxima are necessary for the initiation of shoot regeneration (21,55,56), WUS-RELATED HOMEOBOX5 expression is associated with shoot primordium formation (18), and patterning is clearly an essential phase in the establishment of shoot primordia in root tissues (21,56).…”

“…RPK1 has been reported to function upstream of abscisic acid (ABA) signaling (44) and be involved in diverse processes, such as stress tolerance, senescence, embryonic patterning, and formation of cotyledon primordia (34,36,(45)(46)(47)(48). Assessment of the regeneration rate of two rpk1 mutants in the Col-0 background clearly showed the importance of this gene in regeneration, assigning an additional function to RPK1.…”

The Protein Trio RPK1–CaM4–RbohF Mediates Transient Superoxide Production to Trigger Age-Dependent Cell Death in Arabidopsis

“…RPK1 was identified to be upregulated by ABA and abiotic stresses (Hong et al, 1997) and has been shown to function as a positive regulator of ABA signaling (Osakabe et al, 2005(Osakabe et al, , 2010. Furthermore, RPK1 plays important roles in other developmental processes, including age-dependent cell death (Lee et al, 2011), embryonic pattern formation (Nodine et al, 2007), shoot regeneration (Motte et al, 2014), and cotyledon development (Luichtl et al, 2013). It is uncertain whether ABA, via RPK1, is involved in these developmental processes, but RPK1 in senescence has been shown to depend on ABA (Lee et al, 2011).…”