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

Fiesselmann BS, Luichtl M, Yang X, Matthes M, Peis O, Torres-Ruiz RA - BMC Plant Biol. (2015)

Bottom Line: In strong rpk1 alleles, about 10 % of these (i. e. 1 % of all homozygotes) did not develop a SAM.The 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.The specific cotyledon defect in rpk1 mutants thus sheds light upon the developmental implications of the transition from two cotyledons to one.

View Article: PubMed Central - PubMed

Affiliation: Lehrstuhl für Genetik, Technische Universität München, Wissenschaftszentrum Weihenstephan, Emil-Ramann-Str. 8, D-85354, Freising, Germany. birgit.fiesselmann@gmail.com.

ABSTRACT

Background: In 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.

Results: SAM-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.

Conclusions: The 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.

No MeSH data available.


Related in: MedlinePlus

Model explaining early rpk1-7 defects. a The failure to achieve sufficient RPK1 function (red arrowheads) by redundant genes in the rpk1-7 mutant is stochastic with respect to time and space. Early alterations have more severe effects than late ones on SAM- vs. cotyledon organizing cell groups. b Given are possible expression patterns (blue) of KNAT2p:GUS as an example for a SAM-related gene. c The realization and maintenance of a shoot meristem depends on the precisely localized and concerted expression of all required SAM genes. d Shown are the frequencies of mono- and dicots with and without SAMs/eSMs based mainly on rpk1-7 data (for details see text and Methods). Green spots symbolize auxin maxima. Note that repeated PIN1 polarity and cell division disturbance can cause additional maxima and lobed cotyledons (see [22])
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Fig7: Model explaining early rpk1-7 defects. a The failure to achieve sufficient RPK1 function (red arrowheads) by redundant genes in the rpk1-7 mutant is stochastic with respect to time and space. Early alterations have more severe effects than late ones on SAM- vs. cotyledon organizing cell groups. b Given are possible expression patterns (blue) of KNAT2p:GUS as an example for a SAM-related gene. c The realization and maintenance of a shoot meristem depends on the precisely localized and concerted expression of all required SAM genes. d Shown are the frequencies of mono- and dicots with and without SAMs/eSMs based mainly on rpk1-7 data (for details see text and Methods). Green spots symbolize auxin maxima. Note that repeated PIN1 polarity and cell division disturbance can cause additional maxima and lobed cotyledons (see [22])

Mentions: However, what then causes ectopic SAM gene expression and eSM development? Homozygous rpk1 mutants differ from previous examples where ectopic shoot meristems were induced in transgenic and complex dominant mutation backgrounds respectively [30, 37, 42, 43, 46]. In contrast, rpk1 mutants represent a loss-of-function state and form late SAMs at correct positions or eSMs ectopically on top of cotyledons. The rpk1-7 ectopic shoots, although larger, are reminiscent of epiphyllous inflorescences on foliage leaves in fil-5 yab3-1 mutants [47] and of ectopic leaf buds in as1 mutants [27]. However, none of these genes is mutated in rpk1 plants. The only link to ectopic SAM gene expression (and eSMs) in these mutants is the altered hypocotyl-cotyledon fusion morphology. The probability that eSMs occurred exclusively in morphologically altered SAM-less monocots (6 in 10000; Table 2) just by chance is extremely low (≤10−12). This leads us to a model, which integrates the primary defects of rpk1 mutants, i. e. disturbance of epidermal PIN1 polarity and cell division, and their phenotypes (Fig. 7). In fact, disturbance of PIN1 polarity and auxin homeostasis respectively have been demonstrated to affect initiation of shoot regeneration [39, 48, 49]. Our model takes into account, that due to functional redundancy these defects stochastically scatter along the complete embryo development (Fig. 7). The earlier the rpk1 defects manifest the more severe are the consequences. The extreme is a fused hypocotyl-cotyledon morphology with the loss of the SAM, which is one of the earliest cell commitments in the embryo (Fig. 7). Apparently, the continuous hypocotyl-cotyledon morphology is accompanied by a loss of positional information because post-embryonically a shoot meristem can form at different positions (late SAMs, eSMs). This circumstance is also reflected in variable ectopic SAM gene expression patterns in those SAM-less monocots, which fail to form a shoot meristem (Fig. 7).Fig. 7


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

Fiesselmann BS, Luichtl M, Yang X, Matthes M, Peis O, Torres-Ruiz RA - BMC Plant Biol. (2015)

Model explaining early rpk1-7 defects. a The failure to achieve sufficient RPK1 function (red arrowheads) by redundant genes in the rpk1-7 mutant is stochastic with respect to time and space. Early alterations have more severe effects than late ones on SAM- vs. cotyledon organizing cell groups. b Given are possible expression patterns (blue) of KNAT2p:GUS as an example for a SAM-related gene. c The realization and maintenance of a shoot meristem depends on the precisely localized and concerted expression of all required SAM genes. d Shown are the frequencies of mono- and dicots with and without SAMs/eSMs based mainly on rpk1-7 data (for details see text and Methods). Green spots symbolize auxin maxima. Note that repeated PIN1 polarity and cell division disturbance can cause additional maxima and lobed cotyledons (see [22])
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4492102&req=5

Fig7: Model explaining early rpk1-7 defects. a The failure to achieve sufficient RPK1 function (red arrowheads) by redundant genes in the rpk1-7 mutant is stochastic with respect to time and space. Early alterations have more severe effects than late ones on SAM- vs. cotyledon organizing cell groups. b Given are possible expression patterns (blue) of KNAT2p:GUS as an example for a SAM-related gene. c The realization and maintenance of a shoot meristem depends on the precisely localized and concerted expression of all required SAM genes. d Shown are the frequencies of mono- and dicots with and without SAMs/eSMs based mainly on rpk1-7 data (for details see text and Methods). Green spots symbolize auxin maxima. Note that repeated PIN1 polarity and cell division disturbance can cause additional maxima and lobed cotyledons (see [22])
Mentions: However, what then causes ectopic SAM gene expression and eSM development? Homozygous rpk1 mutants differ from previous examples where ectopic shoot meristems were induced in transgenic and complex dominant mutation backgrounds respectively [30, 37, 42, 43, 46]. In contrast, rpk1 mutants represent a loss-of-function state and form late SAMs at correct positions or eSMs ectopically on top of cotyledons. The rpk1-7 ectopic shoots, although larger, are reminiscent of epiphyllous inflorescences on foliage leaves in fil-5 yab3-1 mutants [47] and of ectopic leaf buds in as1 mutants [27]. However, none of these genes is mutated in rpk1 plants. The only link to ectopic SAM gene expression (and eSMs) in these mutants is the altered hypocotyl-cotyledon fusion morphology. The probability that eSMs occurred exclusively in morphologically altered SAM-less monocots (6 in 10000; Table 2) just by chance is extremely low (≤10−12). This leads us to a model, which integrates the primary defects of rpk1 mutants, i. e. disturbance of epidermal PIN1 polarity and cell division, and their phenotypes (Fig. 7). In fact, disturbance of PIN1 polarity and auxin homeostasis respectively have been demonstrated to affect initiation of shoot regeneration [39, 48, 49]. Our model takes into account, that due to functional redundancy these defects stochastically scatter along the complete embryo development (Fig. 7). The earlier the rpk1 defects manifest the more severe are the consequences. The extreme is a fused hypocotyl-cotyledon morphology with the loss of the SAM, which is one of the earliest cell commitments in the embryo (Fig. 7). Apparently, the continuous hypocotyl-cotyledon morphology is accompanied by a loss of positional information because post-embryonically a shoot meristem can form at different positions (late SAMs, eSMs). This circumstance is also reflected in variable ectopic SAM gene expression patterns in those SAM-less monocots, which fail to form a shoot meristem (Fig. 7).Fig. 7

Bottom Line: In strong rpk1 alleles, about 10 % of these (i. e. 1 % of all homozygotes) did not develop a SAM.The 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.The specific cotyledon defect in rpk1 mutants thus sheds light upon the developmental implications of the transition from two cotyledons to one.

View Article: PubMed Central - PubMed

Affiliation: Lehrstuhl für Genetik, Technische Universität München, Wissenschaftszentrum Weihenstephan, Emil-Ramann-Str. 8, D-85354, Freising, Germany. birgit.fiesselmann@gmail.com.

ABSTRACT

Background: In 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.

Results: SAM-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.

Conclusions: The 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.

No MeSH data available.


Related in: MedlinePlus