Introduction
Hypocotyl growth including elongation and thickening is important for
the emergence of tomato seedlings from soil and resistance to lodging.
In the dark, seedlings undergo skotomorphogenic development including
closed cotyledons, formation of an apical hook and elongated hypocotyls.
In the light, photomorphogenic development results in cotyledon
expansion, leaf development, photosynthesis initiation and reduced
hypocotyl elongation. Many mutants of light signaling components exhibit
defective hypocotyl growth. Loss-of-function mutant of phyB(Phytochrome B ), the red-light receptor, has elongated hypocotyls
(de Lucas et al., 2008; Kim et al., 2016). Phytochrome interacting
factors (PIFs ) are transcription factors downstream of light
signaling to positively regulate hypocotyl elongation, and monogenicPIF mutants have shorter hypocotyls than wild-type plants under
light condition (Huq & Quail, 2002; Kim et al., 2003; Zhong et al.,
2012). Ambient temperature also regulates hypocotyl elongation. High
temperature promotes hypocotyl elongation through the increase of free
IAA in Arabidopsis seedlings (Gray, Ostin, Sandberg, Romano, & Estelle,
1998). PIF4 promotes IAA biosynthesis, and is also required for high
temperature induced hypocotyl elongation (Franklin et al., 2011; Koini
et al., 2009; Stavang et al., 2009). PIF4 specifically binds to the
biologically active Pfr form of phyB, which results in the degradation
of PIF4 and prevents its transcription activity in the hypocotyl
elongation (Huq & Quail, 2002; Park et al., 2012). PhyB-PIF signaling
module also regulates red light-induced hypocotyl elongation under the
warm temperature (Johansson et al., 2014). Blue light inhibits
Arabidopsis hypocotyl elongation requiring the function ofcryptochrome 1 (CRY1 ) and cryptochrome 2(CRY2 ) (Ahmad & Cashmore, 1993). Under blue light, CRY1 directly
interacts with PIF4 to inhibit its transcription activity and represses
the hypocotyl elongation induced by high temperature (Ma et al., 2016).
Plant hormones have diverse and strong impacts on hypocotyl growth.
Overproduction of auxin in plants promotes hypocotyl elongation (Boerjan
et al., 1995; Romano, Robson, Smith, Estelle, & Klee, 1995; Zhao et
al., 2001). Chemical screens identify a new auxin analog named pro-2,4-D
which significantly promotes hypocotyl elongation (Savaldi-Goldstein et
al., 2008). Exogenous application of gibberellins promotes Arabidopsis
hypocotyl elongation under light via regulation of cellular elongation
(Cowling & Harberd, 1999). Ethylene prevents the hypocotyl elongation
in the dark, while promotes hypocotyl elongation in the light (Bleecker,
Estelle, Somerville, & Kende, 1988; Smalle, Haegman, Kurepa, Van
Montagu, & Straeten, 1997). Brassinosteroid (BR) stimulates hypocotyl
elongation of pakchoi (Brassica chinensis cv Lei-Choi) (T. W.
Wang, Cosgrove, & Arteca, 1993) and BR signaling is required for
GA-induced hypocotyl elongation (Bai et al., 2012). Appropriate
endogenous level of Abscisic acid (ABA) is essential for tomato
hypocotyl elongation in the dark, which promotes the endoreduplication
in hypocotyl cells and inhibits cytokinin biosynthesis (Humplik et al.,
2015). Cytokinins inhibit hypocotyl elongation of Arabidopsis seedlings
in the dark, while induce hypocotyl elongation in light-grown
Arabidopsis plants via suppression of ethylene action or auxin transport
(Smets, Le, Prinsen, Verbelen, & Van Onckelen, 2005).
Hypocotyl growth is species- and growth condition-dependent, resulting
from cell division and expansion (Gendreau et al., 1997; Raz &
Koornneef, 2001; H. Wang & Shang, 2020). In Arabidopsis, hypocotyl
growth is exclusively attributed to cell expansion (Boron & Vissenberg,
2014), while both cell division and expansion exist in hypocotyls ofHelianthus annuus (Kutschera & Niklas, 2013). Accurate cell
cycle progression including mitotic cycle and endoreduplication results
in proper cell division and expansion during plant organ growth and
development (De Veylder, Beeckman, & Inze, 2007; Sugimoto-Shirasu &
Roberts, 2003). Cell cycle consists of four major phases, G1, S, G2 and
M, and the progression is governed by the activity of cyclin-dependent
kinases (CDKs)/cyclin protein complex, in which CDK is the catalytic
subunit and cyclin is the regulatory subunit (Inze & De Veylder, 2006).
CDK inhibitors (CKIs) or Kip-related proteins (KRPs) directly bind to
the CDK/cyclin complexes to inhibit CDK activity (De Veylder et al.,
2001; Lui et al., 2000; Sherr & Roberts, 1999; H. Wang, Fowke, &
Crosby, 1997). SIAMESE(SIM)/SIAMESE RELATED (SMR) family proteins are
another type of inhibitors of CDK activity controlling endocycle onset
in Arabidopsis (Churchman et al., 2006; Kasili et al., 2010; Walker,
Oppenheimer, Concienne, & Larkin, 2000). Cell cycle from G2 to M phase
requires E3 ubiquitin ligase complexes Anaphase-promoting
complex/cyclosome (APC/C) to degrade cyclins and inhibit CDK activity
(Fulop et al., 2005; Marrocco, Bergdoll, Achard, Criqui, & Genschik,
2010; Peters, 2006; Sullivan & Morgan, 2007). APC/C is a large protein
complex containing at least 11 different subunits referred as APC1 to
APC11, in which APC2 and APC11 are core components with catalytic
activities. APC/C has two types of activators, cell division cycle
20 (CDC20 ) and CELL CYCLE SWITCH52 (CCS52 ) (Fulop
et al., 2005). Five CDC20 homologs
(CDC20.1 -CDC20.5 ) and three CCS52 homologs
(CCS52A1 , CCS52A2 and CCS52B ) were identified in
Arabidopsis genome. ULTRAVIOLET-B-INSENSITIVE4 (UVI4 ) andOMISSION OF SECOND DIVISION1 (OSD1 ) are two negative
regulators of APC/C, which have functional redundancy in the regulation
of female gametophyte development (Bao & Hua, 2014; Heyman et al.,
2011; Iwata et al., 2011). Either UVI4 or OSD1overexpression leads to reduced plant size, lateral shoots and enhanced
disease resistance (Bao, Yang, & Hua, 2013; Iwata et al., 2011).
Studies on APC/C activities in tomato hypocotyl growth were seldom
reported. Here we accessed roles of the negative APC/C regulatorSlUVI4 and the positive regulator SlCCS52B in hypocotyl
elongation via the modulation of cell cycle progression. High expression
levels of both genes correlated with the robust hypocotyl elongation
when seedlings grow under different lights or on the growth medium
supplemented with MS salts and sugar. Salt, heat and plant hormones
auxin and ethylene treatments affect their transcription distinctly to
modulate hypocotyl elongation via the perturbation of cell cycle
progression. Genetic studies revealed that SlCCS52Boverexpression Arabidopsis plants and SlUVI4 deletion mutants had
defective hypocotyl elongation with enhanced endoreduplication.
Together, our study establishes cellular and genetic connections between
APC/C regulators, cell cycle progression and tomato hypocotyl
elongation.