Class III compensation, represented by<i>KRP2</i>overexpression, depends on V-ATPase activity in proliferative cells

Ferjani, Ali; Ishikawa, Kazuki; Asaoka, Mariko; Ishida, Masanori; Horiguchi, Gorou; Maeshima, Masayoshi; Tsukaya, Hirokazu

doi:10.4161/psb.27204

Cited by 13 publications

(17 citation statements)

References 22 publications

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“…Several compensation-exhibiting mutants have been identified and some of their causal genes have been cloned and functionally characterized ( Horiguchi et al, 2005 ; Ferjani et al, 2007 , 2011 , 2013a ; Kawade et al, 2010 , 2013 ; Hisanaga et al, 2013 ). The cellular dynamics of compensation in aerial lateral organs has been finely dissected and several rules governing triggering of compensation have emerged ( Ferjani et al, 2008 , 2010 , 2013b ; Horiguchi and Tsukaya, 2011 ; Hisanaga et al, 2015 ). In addition, compensation has been subclassified into three conventional classes based on post-mitotic cell expansion patterns ( Ferjani et al, 2013b ).…”

Section: Introductionmentioning

confidence: 99%

“…The cellular dynamics of compensation in aerial lateral organs has been finely dissected and several rules governing triggering of compensation have emerged ( Ferjani et al, 2008 , 2010 , 2013b ; Horiguchi and Tsukaya, 2011 ; Hisanaga et al, 2015 ). In addition, compensation has been subclassified into three conventional classes based on post-mitotic cell expansion patterns ( Ferjani et al, 2013b ). In fact, previous kinematic analyses of cell size dynamics during leaf development show that CCE occurs through three different modes ( Ferjani et al, 2007 ), including class I, when post-mitotic cell expansion rate is enhanced, class II, when the post-mitotic cell expansion period is extended, and class III, when increased cell size occurs during the cell proliferative stage (i.e., before the start of post-mitotic cell expansion; Ferjani et al, 2013b ; Hisanaga et al, 2015 ).…”

Section: Introductionmentioning

confidence: 99%

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Suppressor Screen and Phenotype Analyses Revealed an Emerging Role of the Monofunctional Peroxisomal Enoyl-CoA Hydratase 2 in Compensated Cell Enlargement

et al. 2016

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Efficient use of seed nutrient reserves is crucial for germination and establishment of plant seedlings. Mobilizing seed oil reserves in Arabidopsis involves β-oxidation, the glyoxylate cycle, and gluconeogenesis, which provide essential energy and the carbon skeletons needed to sustain seedling growth until photoautotrophy is acquired. We demonstrated that H+-PPase activity is required for gluconeogenesis. Lack of H+-PPase in fugu5 mutants increases cytosolic pyrophosphate (PPi) levels, which partially reduces sucrose synthesis de novo and inhibits cell division. In contrast, post-mitotic cell expansion in cotyledons was unusually enhanced, a phenotype called compensation. Therefore, it appears that PPi inhibits several cellular functions, including cell cycling, to trigger compensated cell enlargement (CCE). Here, we mutagenized fugu5-1 seeds with 12C6+ heavy-ion irradiation and screened mutations that restrain CCE to gain insight into the genetic pathway(s) involved in CCE. We isolated A#3-1, in which cell size was severely reduced, but cell number remained similar to that of original fugu5-1. Moreover, cell number decreased in A#3-1 single mutant (A#3-1sm), similar to that of fugu5-1, but cell size was almost equal to that of the wild type. Surprisingly, A#3-1 mutation did not affect CCE in other compensation exhibiting mutant backgrounds, such as an3-4 and fugu2-1/fas1-6. Subsequent map-based cloning combined with genome sequencing and HRM curve analysis identified enoyl-CoA hydratase 2 (ECH2) as the causal gene of A#3-1. The above phenotypes were consistently observed in the ech2-1 allele and supplying sucrose restored the morphological and cellular phenotypes in fugu5-1, ech2-1, A#3-1sm, fugu5-1 ech2-1, and A#3-1; fugu5-1. Taken together, these results suggest that defects in either H+-PPase or ECH2 compromise cell proliferation due to defects in mobilizing seed storage lipids. In contrast, ECH2 alone likely promotes CCE during the post-mitotic cell expansion stage of cotyledon development, probably by converting indolebutyric acid to indole acetic acid.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Suppressor Screen and Phenotype Analyses Revealed an Emerging Role of the Monofunctional Peroxisomal Enoyl-CoA Hydratase 2 in Compensated Cell Enlargement

et al. 2016

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“…The size of a plant organ is determined both by the number of cells constituting the organ and by the sizes of the constituent cells ( Horiguchi et al , 2006 ). Compensatory changes in these two parameters are often observed ( Truernit and Haseloff, 2008 ; Larson-Rabin et al , 2009 ; Kawade et al , 2010 ; Ferjani et al , 2013 ; Hisanaga et al , 2013 ), such that genetic alterations changing cell division often lead to changes in cell size that tend to restore a more normal organ size, and vice versa. These observations have led to the hypothesis of ‘compensation’, a formal mechanism by which an organ-level size control manipulates these two parameters to attempt to maintain a constant size ( Tsukaya, 2008 ).…”

Section: Introductionmentioning

confidence: 99%

AINTEGUMENTA and the D-type cyclin CYCD3;1 independently contribute to petal size control in Arabidopsis: evidence for organ size compensation being an emergent rather than a determined property

Randall

Sornay

Dewitte

et al. 2015

Journal of Experimental Botany

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“…It is believed that coordination (involving cell-and non-autonomous pathways) between cell proliferation and differentiation is essential to produce leaves with appropriate shapes and sizes. [6][7][8][9][10][11][12][13][14][15] Nonetheless, despite advances in our understanding of leaf development, flowering stems have not been well-characterized.…”

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Balanced cell proliferation and expansion is essential for flowering stem growth control

Ferjani

Hanai

Gunji

et al. 2015

Plant Signaling & Behavior

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The postembryonic development of aboveground plant organs relies on a continuous supply of cells from the shoot apical meristem. Previous studies of developmental regulation in leaves and flowers have revealed the crucial role of coordinated cell proliferation and differentiation during organogenesis. However, the importance of this coordination has not been examined in flowering stems. Very recently, we attempted to identify regulatory factors that maintain flowering stem integrity. We found that the increased cell number in clavata (clv) mutants and the decreased cell size in de-etiolated (det)3-1 resulted in flowering stems that were thicker and thinner, respectively, than in wild-type (WT) plants. Interestingly, in the cell proliferation- and cell expansion-defective double mutant clv det3-1, the flowering stems often exhibited severe cracking, resulting in exposure of their inner tissues. In this study, further quantification of the cellular phenotypes in the cotyledons and leaves revealed no differences between det3-1 and clv3 det3-1. Together, the above findings suggest that the clv3 mutation in a det3-1 background primarily affects flowering stems, while its effect on other organs is likely negligible. We propose that the coordination between cell proliferation and differentiation is not only important during leaf development, but also plays a role in the growth control of Arabidopsis flowering stems.

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Class III compensation, represented byKRP2overexpression, depends on V-ATPase activity in proliferative cells

Cited by 13 publications

References 22 publications

Suppressor Screen and Phenotype Analyses Revealed an Emerging Role of the Monofunctional Peroxisomal Enoyl-CoA Hydratase 2 in Compensated Cell Enlargement

Suppressor Screen and Phenotype Analyses Revealed an Emerging Role of the Monofunctional Peroxisomal Enoyl-CoA Hydratase 2 in Compensated Cell Enlargement

AINTEGUMENTA and the D-type cyclin CYCD3;1 independently contribute to petal size control in Arabidopsis: evidence for organ size compensation being an emergent rather than a determined property

Balanced cell proliferation and expansion is essential for flowering stem growth control

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