Organ Size Regulation in Plants: Insights from Compensation

The regulation of organ size in higher organisms is a fundamental issue in developmental biology. In flowering plants, a phenomenon called “compensation” has been observed where a cell proliferation defect in developing leaf primordia triggers excessive cell expansion. As a result, final leaf size is not significantly reduced compared to that expected from the reduction in leaf cell numbers. Recent genetic studies have revealed several key features of the compensation phenomenon. Compensation is induced either cell autonomously or non-cell autonomously depending on the trigger that impairs cell proliferation; a certain type of compensation is induced only when cell proliferation is impaired beyond a threshold level. Excessive cell expansion is achieved by either an increased cell expansion rate or a prolonged period of cell expansion via genetic pathways that are also required for normal cell expansion. These results indicate that cell proliferation and cell expansion are coordinated through multiple pathways during leaf size determination. Further classification of compensation pathways and their characterization at the molecular level will provide a deeper understanding of organ size regulation

ANGUSTIFOLIA3 Signaling Coordinates Proliferation between Clonally Distinct Cells in Leaves

SummaryCoordinated proliferation between clonally distinct cells via inter-cell-layer signaling largely determines the size and shape of plant organs [1–4]. Nonetheless, the signaling mechanism underlying this coordination in leaves remains elusive because of a lack of understanding of the signaling molecule (or molecules) involved. ANGUSTIFOLIA3 (AN3, also called GRF-INTERACTING FACTOR1) encodes a putative transcriptional coactivator with homology to human synovial sarcoma translocation protein [5–7]. AN3 transcripts accumulate in mesophyll cells but are not detectable in leaf epidermal cells [8]. However, we found here that in addition to mesophyll cells [5, 6], epidermal cells of an3 leaves show defective proliferation. This spatial difference between the accumulation pattern of AN3 transcripts and an3 leaf phenotype is explained by AN3 protein movement across cell layers. AN3 moves into epidermal cells after being synthesized within mesophyll cells and helps control epidermal cell proliferation. Interference with AN3 movement results in abnormal leaf size and shape, indicating that AN3 signaling is indispensable for normal leaf development. AN3 movement does not require type II chaperonin activity, which is needed for movement of some mobile proteins [9]. Taking these findings together, we present a novel model emphasizing the role of mesophyll cells as a signaling source coordinating proliferation between clonally independent leaf cells

DIFFEOMORPHISM OF AFFINE CONNECTED SPACES WHICH PRESERVED RIEMANNIAN AND RICCI CURVATURE TENSORS

<p>Organ size regulation is dependent on the precise spatial and temporal regulation of cell proliferation and cell expansion. A number of transcription factors have been identified that play a key role in the determination of aerial lateral organ size, but their functional relationship to various chromatin modifiers has not been well understood. To understand how leaf size is regulated, we previously isolated the oligocellula1 (oli1) mutant of Arabidopsis thaliana that develops smaller first leaves than the wild type (WT) mainly due to a reduction in the cell number. In this study, we further characterized oli1 leaf phenotypes and identified the OLI1 gene as well as interaction partners of OLI1. Detailed characterizations of leaf development suggested that the cell proliferation rate in oli1 leaf primordia is lower than that in the WT. In addition, oli1 was associated with a slight delay of the progression from the juvenile to adult phases of leaf traits. A classical map-based approach demonstrated that OLI1 is identical to HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES15 (HOS15). HOS15/OLI1 encodes a homolog of human transducin β-like protein1 (TBL1). TBL1 forms a transcriptional repression complex with the histone deacetylase (HDAC) HDAC3 and either nuclear receptor co-repressor (N-CoR) or silencing mediator for retinoic acid and thyroid receptor (SMRT). We found that mutations in HISTONE DEACETYLASE9 (HDA9) and a switching-defective protein 3, adaptor 2, N-CoR, and transcription factor IIIB-domain protein gene, POWERDRESS (PWR), showed a small-leaf phenotype similar to oli1. In addition, hda9 and pwr did not further enhance the oli1 small-leaf phenotype, suggesting that these three genes act in the same pathway. Yeast two-hybrid assays suggested physical interactions, wherein PWR probably bridges HOS15/OLI1 and HDA9. Earlier studies suggested the roles of HOS15, HDA9, and PWR in transcriptional repression. Consistently, transcriptome analyses showed several genes commonly upregulated in the three mutants. From these findings, we propose a possibility that HOS15/OLI1, PWR, and HDA9 form an evolutionary conserved transcription repression complex that plays a positive role in the regulation of final leaf size.</p

ROTUNDIFOLIA4 Regulates Cell Proliferation Along the Body Axis in Arabidopsis Shoot

Molecular genetics has been successful in identifying leaf- size regulators such as transcription factors, phytohormones, and signal molecules. Among them, a ROTUNDIFOLIA4-LIKE/DEVIL (RTFL/DVL) family of Arabidopsis, genes encoding peptides with no secretion-signal sequence, is unique in that their overexpressors have a reduced number of leaf cells specifically along the proximodistal axis. However, because the RTFL/DVL lack any obvious homology with functionally identified domains, and because of genetic redundancy among RTFL/DVL, their molecular and developmental roles are unclear. In this study we focused on one member in the family, ROTUNDIFOLIA4 (ROT4), and identified the core functional region within it and we found no proteolytic processing in planta. Developmental analysis of leaf primordia revealed that ROT4 overexpression reduces the meristematic zone size within the leaf blade. Moreover, induced local overexpression demonstrated that ROT4 acts as a regulator of the leaf shape via a change in positional cue along the longitudinal axis. Similarly, ROT4 overexpression results in a protrusion of the main inflorescence stem, again indicating a change in positional cue along the longitudinal axis. These results suggest that ROT4 affects the positional cue and cell proliferation along the body axis

Two Nucleolar Proteins, GDP1 and OLI2, Function As Ribosome Biogenesis Factors and Are Preferentially Involved in Promotion of Leaf Cell Proliferation without Strongly Affecting Leaf Adaxial–Abaxial Patterning in Arabidopsis thaliana

Leaf abaxial–adaxial patterning is dependent on the mutual repression of leaf polarity genes expressed either adaxially or abaxially. In Arabidopsis thaliana, this process is strongly affected by mutations in ribosomal protein genes and in ribosome biogenesis genes in a sensitized genetic background, such as asymmetric leaves2 (as2). Most ribosome-related mutants by themselves do not show leaf abaxialization, and one of their typical phenotypes is the formation of pointed rather than rounded leaves. In this study, we characterized two ribosome-related mutants to understand how ribosome biogenesis is linked to several aspects of leaf development. Previously, we isolated oligocellula2 (oli2) which exhibits the pointed-leaf phenotype and has a cell proliferation defect. OLI2 encodes a homolog of Nop2 in Saccharomyces cerevisiae, a ribosome biogenesis factor involved in pre-60S subunit maturation. In this study, we found another pointed-leaf mutant that carries a mutation in a gene encoding an uncharacterized protein with a G-patch domain. Similar to oli2, this mutant, named g-patch domain protein1 (gdp1), has a reduced number of leaf cells. In addition, gdp1 oli2 double mutants showed a strong genetic interaction such that they synergistically impaired cell proliferation in leaves and produced markedly larger cells. On the other hand, they showed additive phenotypes when combined with several known ribosomal protein mutants. Furthermore, these mutants have a defect in pre-rRNA processing. GDP1 and OLI2 are strongly expressed in tissues with high cell proliferation activity, and GDP1-GFP and GFP-OLI2 are localized in the nucleolus. These results suggest that OLI2 and GDP1 are involved in ribosome biogenesis. We then examined the effects of gdp1 and oli2 on adaxial–abaxial patterning by crossing them with as2. Interestingly, neither gdp1 nor oli2 strongly enhanced the leaf polarity defect of as2. Similar results were obtained with as2 gdp1 oli2 triple mutants although they showed severe growth defects. These results suggest that the leaf abaxialization phenotype induced by ribosome-related mutations is not merely the result of a general growth defect and that there may be a sensitive process in the ribosome biogenesis pathway that affects adaxial–abaxial patterning when compromised by a mutation

OLIGOCELLULA1/HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES15 Promotes Cell Proliferation With HISTONE DEACETYLASE9 and POWERDRESS During Leaf Development in Arabidopsis thaliana

Organ size regulation is dependent on the precise spatial and temporal regulation of cell proliferation and cell expansion. A number of transcription factors have been identified that play a key role in the determination of aerial lateral organ size, but their functional relationship to various chromatin modifiers has not been well understood. To understand how leaf size is regulated, we previously isolated the oligocellula1 (oli1) mutant of Arabidopsis thaliana that develops smaller first leaves than the wild type (WT) mainly due to a reduction in the cell number. In this study, we further characterized oli1 leaf phenotypes and identified the OLI1 gene as well as interaction partners of OLI1. Detailed characterizations of leaf development suggested that the cell proliferation rate in oli1 leaf primordia is lower than that in the WT. In addition, oli1 was associated with a slight delay of the progression from the juvenile to adult phases of leaf traits. A classical map-based approach demonstrated that OLI1 is identical to HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES15 (HOS15). HOS15/OLI1 encodes a homolog of human transducin β-like protein1 (TBL1). TBL1 forms a transcriptional repression complex with the histone deacetylase (HDAC) HDAC3 and either nuclear receptor co-repressor (N-CoR) or silencing mediator for retinoic acid and thyroid receptor (SMRT). We found that mutations in HISTONE DEACETYLASE9 (HDA9) and a switching-defective protein 3, adaptor 2, N-CoR, and transcription factor IIIB-domain protein gene, POWERDRESS (PWR), showed a small-leaf phenotype similar to oli1. In addition, hda9 and pwr did not further enhance the oli1 small-leaf phenotype, suggesting that these three genes act in the same pathway. Yeast two-hybrid assays suggested physical interactions, wherein PWR probably bridges HOS15/OLI1 and HDA9. Earlier studies suggested the roles of HOS15, HDA9, and PWR in transcriptional repression. Consistently, transcriptome analyses showed several genes commonly upregulated in the three mutants. From these findings, we propose a possibility that HOS15/OLI1, PWR, and HDA9 form an evolutionary conserved transcription repression complex that plays a positive role in the regulation of final leaf size