Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis

Abstract

The control of cell proliferation during organogenesis plays an important role in initiation, growth, and acquisition of the intrinsic size of organs in higher plants. To understand the developmental mechanism that controls intrinsic organ size by regulating the number and extent of cell division during organogenesis, we examined the function of the Arabidopsis regulatory gene AINTEGUMENATA (ANT). Previous observations revealed that ANT regulates cell division in integuments during ovule development and is necessary for floral organ growth. Here we show that ANT controls plant organ cell number and organ size throughout shoot development. Loss of ANT function reduces the size of all lateral shoot organs by decreasing cell number. Conversely, gain of ANT function, via ectopic expression of a 35S::ANT transgene, enlarges embryonic and all shoot organs without altering superficial morphology by increasing cell number in both Arabidopsis and tobacco plants. This hyperplasia results from an extended period of cell proliferation and organ growth. Furthermore, cells ectopically expressing ANT in fully differentiated organs exhibit neoplastic activity by producing calli and adventitious roots and shoots. Based on these results, we propose that ANT regulates cell proliferation and organ growth by maintaining the meristematic competence of cells during organogenesis.A lthough plant growth is influenced greatly by external environmental factors, it appears that the intrinsic size of plant organs is determined by internal developmental factors. Evidence for intrinsic organ size control is seen by the remarkable uniformity of organ size among individuals within a species (e.g., Arabidopsis thaliana petal size) and by the conspicuous differences in organ size between related species (e.g., A. thaliana versus Brassica napus petal size). Previous genetic analysis has focused primarily on the role of polarized cell elongation in determining organ morphology (1, 2). However, disparity in size of a particular organ (e.g., petal) between species is primarily the result of differences in cell number, not cell size (3). Thus, the intrinsic organ size of a species is determined primarily by organ cell number. Population genetics has indicated that intrinsic plant organ size might be regulated by a polygenic system, and in some species quantitative trait loci that affect plant organ size have been studied (4). However, how intrinsic organ size is genetically controlled, or the nature of the developmental regulators involved in plant organ size control, is not well understood.The total cell number of an organ is determined by the number of divisions of undifferentiated stem cells [i.e., meristematic cells (5)]. During shoot development, lateral organs are initiated as primordia from apical and lateral meristems (6, 7). Although most cells in organ primordia are meristematic and proliferate, cells lose meristematic competence and withdraw from the cell cycle as organs develop. Thus, the maintenance of meristematic competence of cells is ...

The Arabidopsis Auxin-Inducible Gene ARGOS Controls Lateral Organ Size

“…Compared with the undetectable expression in vector control and ARGOS antisense leaves, ANT expression persisted in rosette leaves of 40-day-old 35S-ARGOS plants (Figure 4D). Meanwhile, similar to that in 35S-ANT plants (Mizukami and Fischer, 2000), prolonged expression of CycD3;1 also was detected in 35S-ARGOS leaves ( Figure 4D). However, in 12-day-old rosette leaves, ANT and CycD3;1 transcript levels were comparable in the three genotypes ( Figure 4D).…”

“…Because the phenotypes of ARGOS transgenic plants are similar to those obtained from the loss and gain of function of ANT (Krizek, 1999;Mizukami and Fischer, 2000), we surmised that, like ANT, ARGOS may affect organ cell competence, thus influencing the duration of cell proliferation. To test this hypothesis, we analyzed the expression of ANT and CycD3;1 in fully expanded and young rosette leaves of vector control and ARGOS transgenic plants.…”

“…ANT seems to function as a coordinator of cell proliferation and lateral organ development. Loss of function of ANT reduces the size of leaf and floral organs (Elliott et al, 1996;Klucher et al, 1996;Mizukami and Fischer, 2000), whereas the ectopic expression of ANT increases the sizes of leaf, inflorescence stem, and floral organs. These alterations result mainly from changes in total cell number (Krizek, 1999;Mizukami and Fischer, 2000).…”

“…Loss of function of ANT reduces the size of leaf and floral organs (Elliott et al, 1996;Klucher et al, 1996;Mizukami and Fischer, 2000), whereas the ectopic expression of ANT increases the sizes of leaf, inflorescence stem, and floral organs. These alterations result mainly from changes in total cell number (Krizek, 1999;Mizukami and Fischer, 2000). Further examination reveals that ANT does not affect the growth rate but regulates the extent of organ growth by maintaining the meristematic competence of organ cells, thereby increasing the intrinsic organ size (Mizukami and Fischer, 2000).…”

“…These alterations result mainly from changes in total cell number (Krizek, 1999;Mizukami and Fischer, 2000). Further examination reveals that ANT does not affect the growth rate but regulates the extent of organ growth by maintaining the meristematic competence of organ cells, thereby increasing the intrinsic organ size (Mizukami and Fischer, 2000). To date, little is known about the molecular nature of meristematic compe-tence (Weigel and Jürgens, 2002).…”