Anthocyanins in photoprotection: knowing the actors in play to solve this complex ecophysiological issue

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Though there is compelling evidence for the suite of molecular events regulating the flavonoid branch pathway that leads to anthocyanin biosynthesis (Chen et al., 2019; Naing & Kim, 2018; Saigo et al., 2020), there is still no consensus about the functional significance of anthocyanins in plant–environment interactions (Steyn et al., 2002; Manetas, 2006; Hughes, 2011; Landi et al., 2015, 2021; Gould et al., 2018). This is also the case of colorless flavonoids, hereafter referred to as flavonoids, which accumulate in separate leaf tissues and subcellular organelles to anthocyanins (Pollastri & Tattini, 2011; Agati et al., 2012; Brunetti et al., 2018). Early studies performed on flavonoid-deficient mutants offered conclusive evidence of their ability to provide ultraviolet (UV)-B photoprotection (Li et al., 1993; Lois & Buchanan, 1994; Bieza & Lois, 2001). Their significance as reactive oxygen species (ROS) scavengers and modulators of various developmental processes mediated by ROS and phytohormone signaling (depending on light stress severity) has also been recently ascertained (Hernandez et al., 2009; Agati & Tattini, 2010; Watkins et al., 2017; Muhelemann et al., 2018; Chapman et al., 2019; Agati et al., 2020; Chapman & Muday, 2021). Anthocyanins, differently from flavonoids, have the peculiar capacity of absorbing wavelengths over a wider range, from UV-B to red, of the solar spectrum (Lopes da Silva et al., 2007; Skaar et al., 2014; Aguilar & Hern andez-Brenes, 2015; Nichelmann & Bilger, 2017; Gould et al., 2018), and exclusively accumulate in the vacuoles of epidermal and/or subepidermal cells in red leaves (Hughes & Smith, 2007; Hughes et al., 2007; Hughes, 2011; Boldt et al., 2014; Tattini et al., 2017). They are optimally suited, therefore, to constitute an effective shield against supernumerary photons (thus contributing to the so-called avoidance mechanism), particularly over the visible portion of the solar spectrum, from reaching sensitive targets in the leaf. Inexplicably, after three decades of extensive research, colleagues world-wide are still in dispute about the effective photoprotection provided by anthocyanins in an in planta situation (Hughes, 2011; Landi et al., 2015, 2021; Gould et al., 2018). Two articles, byRenner&Zohner (2019) and by Pena-Novas& Archetti (2020), have recently renewed the debate about the functional significance of anthocyanin biosynthesis in autumn (senescing) leaves. Renner & Zohner (2019) suggested that the primary function of anthocyanins is photoprotection: anthocyanins scavenge ROS and mitigate their formation through light attenuation while senescing leaves are dismantling their photosynthetic apparatus. In support of their hypothesis, Renner & Zohner (2019) reported that cyanic leaves occur more frequently in deciduous tree species inhabiting regions characterized by lower temperatures and higher solar irradiance during autumn/winter, which would render them more vulnerable to severe ‘light stress’ during leaf senescence. This is consistent with the notion that high light and cold stress are among the most effective environmental drivers for biosynthesis of anthocyanins (likely following stressinduced alteration in cellular redox homeostasis – see Page et al. (2012) and Viola et al. (2016) and references cited therein). Anthocyanin-induced photoprotection, in turn, allows senescing cyanic leaves to cope for longer against photooxidative stress and, consequently, to sustain greater nutrient resorption (the so-called photoprotection–resorption hypothesis; sensu Hoch et al., 2003) compared with the anthocyanin-deficient (yellow) counterparts. By contrast, Pena-Novas & Archetti (2020) suggested the ‘coevolution hypothesis’, which posits that the functional significance of autumn leaf color is to provide an honest warning signal to insects that lay eggs in trees during autumn, of high defense investment, and/or low leaf quality (Archetti & Leather, 2005; Archetti et al., 2009). In other words, pests prefer green leaves, simply because red leaves have greater chemical defense than green leaves and/or are lower in nutrient quality (Cooney et al., 2012;Menzies et al., 2016; Pena-Novas & Archetti, 2020). Though we do not dispute the Pena-Novas & Archetti (2020) hypothesis for the functional/adaptive significance of leaf autumn color (Renner & Zohner (2020) have already replied to their argumentations), we strongly challenge the authors’ conclusions that there is not enough evidence in support of an effective photoprotective function of anthocyanins. In fact, their view is simply counterfactual – for recent research articles, see Tattini et al. (2014, 2017), Logan et al. (2015), Zhang et al. (2016, 2018), Zhu et al. (2016), Cooney et al. (2018), Gould et al. (2018), Zheng et al. (2019, 2021), Yu et al. (2019, 2021), Moustaka et al. (2020), and Landi et al. (2021) – and largely based upon superficial observations and reasoning proposed by Manetas (2006). Here, our discussion mostly concerns the anthocyanin’s ability to attenuate visible light, and thereby mitigate photooxidative stress.