Making bigger plants: key regulators of final organ size
Introduction
Organ size can vary quite dramatically between different plant species, even those closely related (Figure 1). However, the final size of leaves and flowers within any particular plant species is quite uniform suggesting a tight control of organ growth. A characteristic final organ size is often achieved even when cell division is disrupted due to mutations or transgenes, a phenomenon termed compensation as the reduction in cell numbers is accompanied by increased cell size [1, 2]. Growth within determinate plant organs (i.e. leaves and flowers) can be considered to consist of two phases; initially cellular growth is coupled with cell division leading to an overall increase in cell number within the developing organ. Subsequently, cell division ceases and further growth of the organ results from cell expansion. In many plant tissues, endoreduplication results in cells that acquire a very large final size (reviewed in [3]).
The mechanisms regulating organ and body size control are just beginning to be revealed in both plants (reviewed in [1, 4, 5, 6, 7, 8, 9]) and animals (reviewed in [10, 11, 12]). In animals, two major pathways that regulate organ size are the target of rapamycin (TOR) pathway that regulates cell growth and the Hippo pathway that regulates cell growth, proliferation, and apoptosis (reviewed in [13, 14]). A number of growth-promoting and growth-restricting factors have now been identified in plants, primarily in Arabidopsis thaliana. However, the identified genes largely define independent genetic pathways making it difficult to develop an integrated model of organ size control. A number of comprehensive reviews on the regulation of plant organ size have been published in the last several years [4, 5, 6, 8]. Here, I highlight several recent advances in the field focusing primarily on genes that are key regulators of organ size. They primarily affect organ size without dramatically affecting organ shape and where determined, their loss and gain of function phenotypes show opposite effects on final organ size (Table 1).
Section snippets
ARF2 is an integration point for auxin and brassinosteroid promoted growth
The plant hormones auxin and brassinosteroids (BRs) are important regulators of plant growth, stimulating both cell division and cell elongation. One means by which auxin controls final organ size is via the novel transcription factor ARGOS (auxin-regulated gene involved in organ size) which acts upstream of AINTEGUMENTA (ANT), a member of the AP2/ERF transcription factor family (Figure 2). Mutations in either gene result in plants with smaller lateral organs while constitutive expression under
KLUH acts noncell autonomously to regulate final organ size
A newly identified promoter of growth, KLUH (KLU), encodes the cytochrome P450 monooxygenase, CYP78A5 (Table 1) [27••]. klu mutants produce thinner stems and smaller leaves and flowers than wild-type plants due to a premature arrest of cell division within developing organs [27••]. Conversely, plants overexpressing KLU produce larger leaves and flowers and thicker stems composed of more cells. Unlike other promoters of growth, KLU mRNA expression is not strictly correlated with proliferating
The TOR pathway in plants links final organ size and environmental conditions
The TOR pathway is a conserved signaling network in mammals, insects, and yeast that regulates cellular growth in response to environmental cues such as nutrient status and stress (reviewed in [13, 34]). TOR, a Ser/Thr kinase of the phosphatidylinositol-3-kinase-related kinase (PIKK) family, is present in two distinct multiprotein complexes (TORC1 and TORC2) that differ in their downstream effectors. TORC1 phosphorylates factors such as p70 ribosomal S6 kinase (S6K) and eIF4E-binding proteins
Ubiquitin-mediated regulation of growth promoters may regulate final organ size
Several known repressors of growth encode proteins associated with ubiquitin-mediated regulation of protein activity. One of these, BIG BROTHER (BB) is an E3 ubiquitin ligase [42]. bb mutants produce larger sepals and petals and have thicker stems than wild-type plants (Table 1). Conversely, plants overexpressing BB produce smaller sepals, petals, and leaves and thinner stems. BB acts to restrict the period of cell proliferation within developing organs, most likely by mediating the
Conclusions
The recent discoveries highlighted here provide new insight in plant organ size control. Despite some important differences, there are similarities between organ size control in plants and metazoans. In both plants and animals, organ size appears to be assessed at the whole organ level rather than the cellular level and noncell-autonomous factors can promote growth throughout a developing organ [27••, 47]. In addition, there are parallels between the TOR-signaling pathway in plants and animals.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
I thank John Nelson and Alan Weakly for the Hypericum photo. I apologize to colleagues whose work could not be discussed due to space constraints. Work in my laboratory is supported by US Department of Energy grant 98ER20312.
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