https://orcid.org/0000-0002-7232-5889
The organic compound malate has a large impact on the taste of many of our most popular fruits, for example grapes (Vitis vinifera), tomatoes (Solanum lycopersicum), and in particular apples (Malus domestica). The amount of malate in apples determines how tart (sour) or how sweet we perceive their taste. Taste preference is highly individual, with some people enjoying crisp and sour apples while others prefer apples with a mild sweetness. In addition to taste, it was previously shown that malate accumulation and apple pigmentation share a connection, which explains why we associate bright green apples with tartness and deep red ones with sweetness (Fig. 1; Hu et al., 2016). Apple breeding has produced a large number of varieties, which generally produce either sweeter or tarter fruits (Xu et al., 2012; Etienne et al., 2013).
Nutrient availability, in particular nitrate availability, influences the taste of apples and other fruits. Very low nitrate leads to a sour and tart taste, while moderately high nitrate results in sweeter and mild apples. The BTB-TAZ domain protein MdBT2 is now identified as a key regulator connecting nitrate signaling, vacuolar acidification, and malate accumulation. MdBT2 directly interacts with key transcription factors that regulate the expression of vacuolar proton pumps and the malate channel MdALMT9. Expression of these genes influences the amount of malate stored in vacuoles, which in turn determines the tartness or sweetness of apples and many other fruits. Adapted from Zhang et al. (2020); image generated with biorender.
Apart from the variety, many environmental factors also affect malate accumulation. Therefore, coloration and taste within one variety can vary, and sometimes you bite into your favorite apple and it does not taste as expected. One of the factors influencing malate accumulation in fruits is nutrient availability (Etienne et al., 2013). In particular, high nitrate availability is known to affect fruit tartness (Spironello et al., 2004), but it was not known if there is a regulatory signaling mechanism connecting malate and nitrate accumulation or if the two anions simply compete for storage space in the vacuole through independent signaling pathways (Fig. 1).
In this issue of Plant Physiology, Zhang et al. (2020) identified the key regulator protein MdBT2 (BTB-TAZ containing protein2). MdBT2 provides a direct link between nitrate availability, vacuolar pH, and malate accumulation. MdBT2 is a nitrate-responsive protein that physically interacts with an important transcription factor, MdClbHLH1. The MdClbHLH1 transcription factor regulates the expression of key genes involved in malate accumulation, such as the vacuolar proton pumps V-ATPase and V-PPase and the vacuolar malate channel MdALMT9 (Fig. 1; Xu et al., 2012; Hu et al., 2016; Ma et al., 2019; Li et al., 2020).
Under high/moderate nitrate, MdBT2 activity leads to the ubiquitination and degradation of MdClbHLH1 and, ultimately, to higher vacuolar pH and lower malate concentrations. Low nitrate or repression of MdBT2, on the other hand, leads to an increase in MdALMT9 and proton pump gene expression, increasing malate accumulation capacity. This response is nitrate specific; other inorganic anions such as chloride did not have the same effect (Zhang et al., 2020).
The novel molecular network identified by Zhang et al. (2020) provides a key insight on how nitrate signaling, vacuolar acidification, and malate accumulation are regulated in plants. Additionally, the identification of a protein at the interconnection of nitrate sensing and malate accumulation provides a novel target for breeding strategies, not only in apples but also in other crops, such as tomatoes, with the goal to optimize fruit quality and taste. Employing this new knowledge on the molecular mechanism, connecting nutrient supply and fruit taste, we might be able to ensure that we can enjoy our apples as tart or as sweet as each of us prefers.
LITERATURE CITED
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Senior author.
