The transcriptional regulation of plant pigments
The transcriptional regulation of anthocyanins in fruit has been well
documented: at its core is a TF complex, termed the MYB-bHLH-WD40 (MBW)
complex (Allan, Hellens & Laing 2008). The MYB component is derived
from the subgroup (SG) 6 class of MYBs (as defined by Stracke et al.
(2001) as opposed to the SG5 MYBs, which control proanthocyanidins) and
has been characterised in many fruit species (Albert et al. 2014;
Jaakola 2013). The MYBs are expressed in ripening fruit and activate
either the whole biosynthetic pathway or a subset of genes in the
pathway. Examples of activators include FaMYB10 and FvMYB10 in
strawberry (Lin-Wang et al. 2014; Medina-Puche et al.2014), MYB10 in nectarine (Prunus persica ) (Ravaglia et
al. 2013), VmMYBA in bilberry (Vaccinium myrtillus ) (Karppinenet al. 2021), PpMYB10.1 in peach (Prunus persica ) (Rahim,
Busatto & Trainotti 2014), VcMYBA1 in blueberry (VacciniumSection Cyanococcus ) (Plunkett et al. 2018) and MYB114 in
pear (Pyrus bretschneideri ) (Yao et al. 2017). MYBs can
also act as repressors of anthocyanin, such as the SG4 MYBs, FaMYB1 from
strawberry (Aharoni et al. 2001) and MdMYB16 from apple
(Malus domestica ) (Xu et al. 2017), as recently reviewed
by LaFountain & Yuan (2021). There is increasing evidence for the
interactions of different types of MYBs on anthocyanin regulation, such
as the co-ordinated actions of MYBA1 and MYBPA1.1 in blueberry (Laffertyet al. 2021). Transcriptional regulation of anthocyanin is not
restricted to the MBW complex: other TFs, such as MADs VmTRD4 in
bilberry (Jaakola et al. 2010) and PpNAC1 in peach (Zhou et
al. 2015) have been shown to have regulatory control. This TF-mediated
control of pigments occurs in response to both developmental cues, but
also environmental stresses.
Carotenoid biosynthesis is stimulated by the presence of ROS (Panet al. 2009). Stress perceived in the leaves can trigger
responses in the fruit, for example, the incidence of high light in
leaves of citrus leads to increases in carotenoids in the fruit
(Poiroux‐Gonord et al. 2013). Many TFs have been associated with
carotenoid biosynthesis as part of the fruit ripening cascade, but the
evidence for there being master transcriptional regulators of carotenoid
pigments is less clear cut than for anthocyanins (Stanley & Yuan 2019).
A number of TFs have recently been shown to control at least parts of
the pathway. In citrus, the AGAMOUS-LIKE MADS TF, CsMADS6, was shown to
activate the promoter of LCYb1 and drive the expression of
carotenoid pathway genes PSY , PDS and CCD1, while
repressing transcription of LCYE and so increasing the flux towards
β-carotene (Lu et al. 2018). Another TF in citrus, CrMYB68,
negatively regulates the expression of beta-carotene hydroxylase (BCH),
controlling the α- and β-branches of carotenoid biosynthesis (Zhuet al. 2017). A MYB from kiwifruit (Actinidia chinensis
var. deliciosa ), MYB7, was reported to activate the promoter ofLCYb and in heterologous systems elevated expression ofPSY , PDS and ZDS to drive carotenoid accumulation
(Ampomah-Dwamena et al. 2019). In papaya, two other TF classes
have been implicated in regulating carotenoids: CpbHLH1 and CpbHLH2
repress and activate respectively the promoters of CYCB and LCYB, while
the NAC TFs, CpNAC1 and CpNAC2, bind the promoters of PDS (NAC1) and
PDS, ZDS, LYCE and BCH (NAC2) (Fu et al. 2016; 2017). The
greatest body of work on the transcriptional control of carotenoids has
been carried out in tomato where the major ripening MADS TFs, Tomato
AGAMOUS-LIKE (TAGL1, homologous to CsMADS6), Ripening Inhibitor (RIN),
FRUITFULL1 (FUL1) and FUL2 exert largely positive effects on the
carotenoid pathway, as reviewed in Stanley & Yuan (2019).