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Keywords:

  • cell cycle;
  • crop performance;
  • development;
  • growth;
  • Nicotiana tabacum (tobacco);
  • pistil;
  • plant reproduction

Plant development takes place almost entirely after embryogenesis in contrast to most animals in which the final body plan is laid out during embryogenesis. Plants therefore are able to respond to changes in biotic and abiotic conditions by adapting their body plan. This requires not only a high level of plasticity on both the cellular and molecular level but also a tight regulation of cell division and growth. These aspects indicate differences in the integration of growth and cell division between animals and plants and would predict the existence of plant-unique factors (Dewitte & Murray, 2003; De Veylder et al., 2007). Although the core cell cycle machinery is in essence the same in all eukaryotes, it has become clear that such plant-specific factors are pivotal for plant development (Nieuwland et al., 2009b). In this issue of New Phytologist, DePaoli et al. (pp. 882–895) describe a novel protein, SCI1 (stigma/style cell cycle inhibitor 1), which may well serve the role of specific cell cycle regulator for pistil development in Nicotiana tabacum (tobacco). The pistil, typically consisting of stigma, style and ovary (see Fig. 1), is the female reproductive organ of the flower in angiosperms. Its proper development is essential for successful plant reproduction. The stigma captures the pollen containing the sperm cells. The pollen forms a tube which grows a considerable distance through stigma and style to reach an ovule in the ovary, after which sperm cells are released for fertilization followed by seed development. Results described in DePaoli et al. suggest that SCI1 acts as an inhibitor of cell division and is specifically involved in the development of tobacco pistils.

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Figure 1. (a) Suppression of SCI1 expression by RNA interference (SCI1Ri) during tobacco flower development results in significantly longer styles and swelling of the stigma at pistil maturity. The spatial separation between stamen and pistil will have a negative effect on seed set in this self pollinating species, being more dependent on visits of its pollinators. (b) SCI1 expression is detectable in the stigma secretory zone (SSZ) and style transmitting tissue (STT). At stage four of flower/pistil development SCI1 expression is mainly detectable in the smaller cells at the boundary (dark purple) between SSZ/STT (light purple) and surrounding ground parenchyma tissue. (c) Photograph illustrating the positioning of stigma/style relative to the anthers in a wild-type tobacco flower (photograph courtesy of Barend H. J. de Graaf).

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‘It is remarkable that a single gene can have such dramatic effects on the pollination strategy of a plant.’

Plant CDK inhibitors

  1. Top of page
  2. Plant CDK inhibitors
  3. SCI1 as a potential novel plant-specific cell cycle inhibitor
  4. Cell cycle regulation, pistil size and plant reproduction
  5. Cell cycle regulation and plant performance
  6. References

In plants there are a large number of genes encoding core cell cycle factors including cyclin-dependent kinases (CDKs) which control progression through the cell cycle (Menges et al., 2005). CDK activity is dependent on the binding of regulatory proteins called cyclins whereas binding of inhibitory proteins can inactivate CDK. Plant CDK inhibitors, called ICKs or KRPs, have a small region of homology to the animal KIP/CIP inhibitors (therefore called Kip-related protein, KRP; De Veylder et al., 2001). All seven ICK/KRP homologues in Arabidopsis are able to interact with cyclins and inhibit cyclin-dependent kinase A (CDKA) activity at least in vitro and overexpression of these proteins leads to reduced cell division. In general, overexpression of ICK/KRPs inhibits growth in terms of plant and organ size but this effect is often compensated by an increase in cell sizes generating fewer but larger cells in an organ (Wang et al., 2008). Almost all data on developmental roles of ICK/KRPs are based on overexpression although recently it was shown that low levels of KRP2 are essential for the correct nuclear localization of the D-type cyclin CYCD2;1, indicating a role as a scaffold for cyclin–CDKA interaction (Sanz et al., 2011). Furthermore, because these cell cycle inhibitors show both cell and cell cycle specific expression and because the expression of at least two ICK/KRPs is regulated through proteasome-dependent destruction, they potentially play important roles in plant development. Another family of plant-specific cell cycle inhibitors is comprised of SIAMESE (SIM) and SIAMESE-related (SMR) proteins (Churchman et al., 2006; Peres et al., 2007). These are distantly related to the ICK/KRPs, sharing the cyclin-binding motif, and interact with both CDKA and D-type cyclins. As observed for ICK/KRPs, overexpression of SIM results in a strong inhibition of cell division activity leading to dwarfed plants with enlarged cells. However, in comparison to ICK/KRPs, much less is known about the functions and regulation of SIM/SIMR proteins. In this issue, DePaoli et al. propose that SCI1 represents a new cell division inhibitory factor which shows both similar and distinct features compared with other known cell cycle inhibitors.

SCI1 as a potential novel plant-specific cell cycle inhibitor

  1. Top of page
  2. Plant CDK inhibitors
  3. SCI1 as a potential novel plant-specific cell cycle inhibitor
  4. Cell cycle regulation, pistil size and plant reproduction
  5. Cell cycle regulation and plant performance
  6. References

SCI1 is a small protein identified in a screen to isolate genes specifically or preferentially expressed in the pistil of tobacco. One specific region of SCI1 shares homology with ICK/KRP proteins leading DePaoli et al. to investigate its function in pistil development by modulation of SCI1 expression. Reduction of SCI1 expression by RNA interference (RNAi) leads to an increase in style length and swelling of the stigma (Fig. 1) due to an increase in cell number in both organs but without a clear reduction of cell size. Conversely, overexpression of SCI1 by the constitutive 35S promoter leads to reduced cell division and growth in the pistil. Interestingly, these effects are restricted to the pistil. By contrast, it has been shown that ectopic overexpression of ICK/KRP and SIM proteins leads to a systemic reduction in cell division and growth which indicates that SCI1 either acts through another pathway or requires a specific factor only present in the tobacco pistil. Furthermore, overexpression of SCI1 does not induce larger cell sizes, a compensatory effect seen when ICK/KRP proteins are overexpressed (Wang et al., 2008) or when cyclin expression levels are reduced, both leading to reduced CDKA activity (Dewitte et al., 2007; Nieuwland et al., 2009a). Elucidating how constitutive overexpression of SCI1 can function in such a tissue specific manner (and without affecting cell sizes) is clearly an important question that needs to be addressed in future studies.

The effect of modulation of SCI1 levels on organ size and cell number does suggest that SCI1 regulates the cell cycle in the stigma and style but further experiments would be needed to show a direct link between SCI1 and the cell cycle. In particular, association with the core cell cycle components cyclin and CDK would need to be proven and maybe overexpression of a mutant form of SCI1 lacking the putative cyclin-binding domain could prove the necessity of this domain for the function of SCI1. Furthermore, SCI1 overexpression remains to be confirmed at the protein level for different tissues as some cell cycle inhibitors, including at least one KRP, are post-translationally regulated by proteolysis (Verkest et al., 2005; Jakoby et al., 2006; Sanz et al., 2011). Nevertheless, the data presented by DePaoli et al. support the hypothesis that SCI might represent a new type of plant-specific cell cycle inhibitors. This leads to the intriguing possibility that the family of CDK inhibitor proteins is larger than previously anticipated and includes regulators acting in a tissue specific manner.

Importantly, the presence of SCI1 homologous genes is widespread and can be found in dicots, including grapevine and Arabidopsis, and in monocots such as barley and rice. Expression analysis of the Arabidopsis SCI1 homolog, At1g79200, shows a very similar expression pattern (Arabidopsis eFP Browser) compared with tobacco SCI1, however, the highest level of expression is found in the shoot apical meristem (SAM). Perhaps an investigation of Arabidopsis mutants in SCI1 homologs will help further define the biological role of these proteins and how prevalently they are used in plant growth and development.

Cell cycle regulation, pistil size and plant reproduction

  1. Top of page
  2. Plant CDK inhibitors
  3. SCI1 as a potential novel plant-specific cell cycle inhibitor
  4. Cell cycle regulation, pistil size and plant reproduction
  5. Cell cycle regulation and plant performance
  6. References

Regulated progression through the cell cycle is essential for the development of the male and female gametophytes (pollen and embryo sac, respectively). Many genes known to affect male and female gametophyte development act by arresting the cell cycle (Borg et al., 2009; Yang et al., 2010). Unlike wild-type flowers where pistil and stamens are of similar length, the stigma in SCI1-suppressed flowers described by DePaoli et al. is positioned well above the anthers (see Fig. 1). This change in spatial separation between male and female reproductive organs results in a change in pistil function: in these plants fewer seeds will originate from self pollination and more seeds from cross pollination by the activity of visiting pollinators. It is remarkable that a single gene can have such dramatic effects on the pollination strategy of a plant. This consideration apparently led DePaoli et al. to hypothesize that SCI1 orthologs might be involved in regulating style length in plants exhibiting heterostyly, a mechanism preventing self-fertilization, thus promoting the genetic diversity of a population. In heterostylous species an inherited discontinuous pattern of variation exists in the population with discrete floral morphs differing, amongst others, in style length (Barrett et al., 2000). The morph phenotype is genetically linked to genes located at the S-locus resulting in heteromorphic self-incompatibility. Although heterostyly has been extensively studied, the genes involved have not yet been identified. It should be noted though that differences in style lengths appear to be predominantly associated with the presence of longer cells in the style (Heslop-Harrison et al., 1981; Webster & Gilmartin, 2006) rather than to differences in cell number.

Cell cycle regulation and plant performance

  1. Top of page
  2. Plant CDK inhibitors
  3. SCI1 as a potential novel plant-specific cell cycle inhibitor
  4. Cell cycle regulation, pistil size and plant reproduction
  5. Cell cycle regulation and plant performance
  6. References

Tight regulation of the cell cycle machinery is of fundamental importance for plants as plant growth and development relies on the temporally and spatially controlled generation of new cells. Detailed knowledge of the plant cell cycle, in particular its regulation in the context of developmental pathways and adaptation to changing environmental conditions, provides opportunities for future applications. For instance, cell cycle regulators that determine organ size in plants could lead to the development of biotechnological tools to increase the amount of lignocellulosic biomass in dedicated energy crops like switchgrass and Miscanthus. Likewise, altering plant architecture, such as increasing the number of tillers, flowers and seeds, through the modulation of the cell cycle would open new perspectives in the breeding or engineering of food crops with improved yield. Several proof of principle studies involving cell cycle regulators, such as the Arabidopsis anaphase promoting complex (APC) subunit AtCDC27a (Rojas et al., 2009) and the Cell Number Regulator 1 (CNR1) (Guo et al., 2010) have shown that both plant architecture and yield can be affected by their expression levels. Moreover, it has been suggested that CDK inhibitors might be involved in linking cell cycle activity and environmental stimuli (Skirycz & Inzé, 2010), which could be exploited for the development of crops that produce significant yields in suboptimum growth conditions.

In summary, DePaoli et al. provided data suggesting SCI1 represents a novel plant-specific CDK inhibitor with a specific role during pistil development in tobacco. It is clear that the identification and detailed functional characterization of new cell cycle regulators, like SCI1, is essential in constructing the complex cell cycle regulatory network in plants. This together with a much deeper understanding of how plant growth and developmental signals as well as environmental cues integrate with the cell cycle machinery is required to fully explore its potential to improve crop performance.

References

  1. Top of page
  2. Plant CDK inhibitors
  3. SCI1 as a potential novel plant-specific cell cycle inhibitor
  4. Cell cycle regulation, pistil size and plant reproduction
  5. Cell cycle regulation and plant performance
  6. References
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