Plant organs grow to characteristic sizes that are genetically controlled. In animals, signaling by mobile growth factors is thought to be an effective mechanism for measuring primordium size, yet how plants gauge organ size is unclear. Here, we identify the Arabidopsis cytochrome P450 KLUH (KLU)/CYP78A5 as a stimulator of plant organ growth. While klu loss-of-function mutants form smaller organs because of a premature arrest of cell proliferation, KLU overexpression leads to larger organs with more cells. KLU promotes organ growth in a non-cell-autonomous manner, yet it does not appear to modulate the levels of known phytohormones. We therefore propose that KLU is involved in generating a mobile growth signal distinct from the classical phytohormones. The expression dynamics of KLU suggest a model of how the arrest of cell proliferation is coupled to the attainment of a certain primordium size, implying a common principle of size measurement in plants and animals.
Organ growth up to a species-specific size is tightly regulated in plants and animals. Final organ size is remarkably constant within a given species, suggesting that a species-specific size checkpoint terminates organ growth in a coordinated and timely manner. Phytohormones influence plant organ size, but their precise functions in size control are unclear because of their pleiotropic and complex developmental roles. The Arabidopsis transcription factors AINTEGUMENTA and JAGGED promote organ growth by maintaining cellular proliferation potential. Loss of the Antirrhinum transcription factor CINCINNATA causes leaf overgrowth, yet also leads to a highly abnormal leaf shape. Thus, no dedicated factor that limits the final size of plant organs has been isolated. Here, we identify the novel RING-finger protein BIG BROTHER (BB) as a repressor of plant organ growth. Small changes in BB expression levels substantially alter organ size, indicating a central regulatory role for BB in growth control. Recombinant BB protein has E3 ubiquitin-ligase activity that is essential for its in vivo function, suggesting that BB acts by marking cellular proteins for degradation. Our data indicate that plants limit the duration of organ growth and ultimately organ size by actively degrading critical growth stimulators.
Seed development in plants involves the coordinated growth of the embryo, endosperm, and maternal tissue. Several genes have been identified that influence seed size by acting maternally, such as AUXIN RESPONSE FACTOR2, APETALA2, and DA1. However, given the lack of gain-of-function effects of these genes on seed size, it is unclear whether their activity levels are limiting in WT plants and whether they could thus be used to regulate seed size in development or evolution. Also, whether the altered seed sizes reflect local gene activity or global physiological changes is unknown. Here, we demonstrate that the cytochrome P450 KLUH (KLU) regulates seed size. KLU acts locally in developing flowers to promote seed growth, and its activity level is limiting for seed growth in WT. KLU is expressed in the inner integument of developing ovules, where it non-cell autonomously stimulates cell proliferation, thus determining the growth potential of the seed coat and seed. A KLU-induced increase in seed size leads to larger seedlings and higher relative oil content of the seeds. Genetic analyses indicate that KLU acts independently of other tested maternal factors that influence integument cell proliferation. Thus, the level of KLU-dependent growth factor signaling determines size in ovules and seeds, suggesting this pathway as a target for crop improvement.Arabidopsis ͉ clonal analysis ͉ cytochrome P450 ͉ seed growth S eed size in higher plants is an important trait with respect to ecology and agriculture (1). For example, larger seeds are less easily dispersed, but offer the germinating seedling a larger supply of nutrients, thus increasing its competitiveness during seedling establishment and tolerance to adverse environmental conditions. At the same time, limited resources in the mother plant generally cause a tradeoff between the number and size of the seeds produced (2). As for agriculture, increasing seed size has been a crucial contributor to the yield increases in crop plants during domestication (3).Seeds are formed by the coordinated growth of maternal sporophytic and zygotic tissues (4). The zygotic tissues are the result of double fertilization, with one sperm cell fertilizing the diploid central cell to yield the triploid endosperm and the other sperm cell fertilizing the haploid egg cell to give rise to the diploid embryo. These maternal gametes lie within the embryo sac that develops in the nucellus region of the ovule (5). The nucellus is surrounded by the integuments, protective organs that form the maternal component of the mature seed after fertilization, the seed coat (6).The size of seeds is known to be influenced by parent-of-origin effects, with a paternal genome excess causing seed overgrowth, whereas a maternal genome excess reduces seed size (7). In addition, recent genetic studies in the model species Arabidopsis thaliana and rice have identified a number of factors affecting seed size by acting in the maternal and/or zygotic tissues. Among the zygotically acting factors, a small cascade of genes ...
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