Ectopic shoot meristem generation in monocotyledonous rpk1 mutants is linked to SAM loss and altered seedling morphology

Abstract

BackgroundIn dicot Arabidopsis thaliana embryos two cotyledons develop largely autonomously from the shoot apical meristem (SAM). Recessive mutations in the Arabidopsis receptor-like kinase RPK1 lead to monocotyledonous seedlings, with low (10 %) penetrance due to complex functional redundancy. In strong rpk1 alleles, about 10 % of these (i. e. 1 % of all homozygotes) did not develop a SAM. We wondered whether RPK1 might also control SAM gene expression and SAM generation in addition to its known stochastic impact on cell division and PINFORMED1 (PIN1) polarity in the epidermis.ResultsSAM-less seedlings developed a simple morphology with a straight and continuous hypocotyl-cotyledon structure lacking a recognizable epicotyl. According to rpk1’s auxin-related PIN1 defect, the seedlings displayed defects in the vascular tissue. Surprisingly, SAM-less seedlings variably expressed essential SAM specific genes along the hypocotyl-cotyledon structure up into the cotyledon lamina. Few were even capable of developing an ectopic shoot meristem (eSM) on top of the cotyledon.ConclusionsThe results highlight the developmental autonomy of the SAM vs. cotyledons and suggest that the primary rpk1 defect does not lie in the seedling’s ability to express SAM genes or to develop a shoot meristem. Rather, rpk1’s known defects in cell division and auxin homeostasis, by disturbed PIN1 polarity, impact on SAM and organ generation. In early embryo stages this failure generates a simplified monocotyledonous morphology. Once generated, this likely entails a loss of positional information that in turn affects the spatiotemporal development of the SAM. SAM-bearing and SAM-less monocotyledonous phenotypes show morphological similarities either to real monocots or to dicot species, which only develop one cotyledon. The specific cotyledon defect in rpk1 mutants thus sheds light upon the developmental implications of the transition from two cotyledons to one.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0556-8) contains supplementary material, which is available to authorized users.

Receptor-like protein kinases in plant reproduction: Current understanding and future perspectives

“…At the heart stage, both the embryo and suspensor of the rpk1 toad2 mutant undergo abnormal morphogenesis, resulting in impaired embryos typically arrested at the late globular stage with a characteristic toadstool shape ( Nodine et al., 2007 ). Moreover, RPK1 and TOAD2 are required to specify cell types of the apical embryonic domain that produces cotyledon primordia ( Nodine and Tax, 2008 ; Fiesselmann et al., 2015 ). Some rpk1 seedlings miss one cotyledon due to disturbed PIN1 polarity and auxin homeostasis in defective embryos at early developmental stages ( Luichtl et al., 2013 ).…”

Natural Variation in Plant Pluripotency and Regeneration

“…Notably, the RPK1 homolog RPK2 regulates WUS expression to control SAM maintenance, and, although this function is not conserved in RPK1 [ 89 ], the two proteins show redundancy during embryogenesis and their sequences mainly differ in the kinase domain [ 81 , 86 ], indicating that they might simply respond to different external cues. Nonetheless, SAM-less monocotyledonous rpk1 mutants are capable of expressing shoot markers and occasionally regenerate ectopic shoot meristems [ 90 ]. Motte et al further showed that early and late regeneration characteristics are poorly correlated, indicating that the shoot organogenetic process can be inhibited at several intermediate stages and chlorophyll maturation does not ensure successful shoot determination [ 11 , 81 ].…”