Environmental shifts have important impacts on the functional traits and bioactive products of medicinal crop Cornus officinalis

Highlights

• Shifts of temperature and precipitation in March are critical for loganin content.

• Environmental shift has opposite effects on fruit weight and ingredient contents.

• Bioactive products have quicker response to environment than functional traits.

• Different bioactive products are correlated and have similar response to environment.

• Introduced regions with similar environment are beneficial for crop yield and product.

Abstract

Environmental gradients play important roles in shaping the diversity of functional traits of crops. Therefore, it is imperative to reveal how crops respond to environmental shifts. In this study, a ten-year investigation (from 2008 to 2018) of an important medicinal crop, dogwood (Cornus officinalis Sieb. et Zucc.), was conducted to reveal the effects of environmental shifts on crop functional traits and bioactive products. The C. officinalis plants originated from three main producing areas were cross-regionally introduced to study area. The key environmental factors of the three original regions (ORs) and the introduced region (IR) were monitored. The functional traits and bioactive products of C. officinalis were estimated. Furthermore, the correlations among functional traits, bioactive products, and environmental factors were analyzed. The results showed that there were significant differences between functional traits and bioactive products of C. officinalis in ORs and in IR (P < 0.01). Further correlation analysis showed that 100-fruit weight was negatively correlated with both average minimum temperature and average precipitation in March (P < 0.01). The changes of loganin content was positively correlated with those of average minimum temperature and average precipitation in March (P < 0.05). Collectively, the above findings indicate that environmental shifts (e.g., average precipitation in March) play important roles in C. officinalis bioactive products. The potential introduced regions with similar environment conditions are beneficial for yield and quality of C. officinalis. These results will provide valuable references for understanding the effects of climate change on functional traits and bioactive products of medicinal crops.

Introduction

Plant functional traits are shaped by both genotypes and environmental conditions (Sultan, 2000). Environmental changes have important effects of altering the habitats in which plants grow and develop. Accordingly, plant species can adjust to these novel conditions through phenotypic plasticity, adapt through natural selection or migrate to follow conditions to which they are adapted (Nicotra et al., 2010). Specifically, plant growth and biosynthesis of secondary metabolites are significantly affected by environmental factors (Ashraf et al., 2018). Changes in environmental conditions can rapidly shift allele frequencies in populations of species as well as the content of secondary metabolites with relatively short generation time (Kessler and Kalske, 2018). In recent decades, such changes have been bringing serious issues regarding the growth and yield of industrial crops globally (Cao et al., 2020; Huang et al., 2019; Challinor et al., 2014; Tubiello et al., 2007). Therefore, it is imperative to reveal how crops respond to environmental shifts under global climatic change.

Dogwood (Cornus officinalis Sieb. et Zucc.) is a perennial deciduous tree in the Cornaceae family and its dried pericarp is used as a famous traditional Chinese medicine (TCM) in China (Yang et al., 2019; Bai et al., 2014; Cao et al., 2014) (Fig. 1). In history, C. officinalis is considered as one of the most important Chinese medicinal materials included in nearly 300 classical prescriptions (Huang et al., 2018). It has been described with efficient treatments of replenishing liver and kidney, and removing phlegm and blood stasis in the Pharmacopoeia of the People's Republic of China (National Pharmacopoeia Commission, 2015). Modern pharmacological studies have shown that C. officinalis contains abundant bioactive products including sugars, organic acids, iridoid glycosides and saponins in fruits (Huang et al., 2018; He et al., 2017; Yin et al., 2016; Xie et al., 2012). Specifically, it has been confirmed that the cornel iridoid glycosides (CIGs, e.g. loganin, morroniside, sweroside, cornuside, etc.) in the dried pericarp of C. officinalis have effective pharmacological activities in the treatment of diabetes, hypertension, inflammation, arteriosclerosis, neurological disorders and apoptosis (Zhang et al., 2020; Sharp-Tawfik et al., 2019; Qu et al., 2019; Chen et al., 2016; Ma et al., 2014; Cao et al., 2013; Jiang et al., 2012; Park et al., 2011; Yao et al., 2009). Meanwhile, recent studies have shown that the protocatechuic acid in C. officinalis has good therapeutic effects against hepatitis B virus (HBV), and the 5-hydroxymethylfurfural has pharmacological activities of protection of liver and kidney and anti-oxidation (Du et al., 2018; Dai et al., 2017). Up to date, the genomic regulation of the above bioactive products in C. officinalis have been well documented in our previous studies (Yang et al., 2019; Bai et al., 2018). However, how the biosynthesis of these bioactive products was affected by environmental factors remains unknown. Further studies are needed to investigate the relationship between bioactive products and environmental conditions for C. officinalis.

The cultivation regions of C. officinalis are mainly distributed in Foping and Danfeng of Shaanxi province, Xixia and Nanzhao of Henan province, and Lin'an and Chun'an of Zhejiang province in China (Cao et al., 2016; Li et al., 2012). In terms of geographical location, Foping and Xixia are located at the same latitude (33°30′N ∼ 33°36′N) in the Qinling-Funiu Mountain, while Lin’an lies at a southward latitude (30°01′N) in Tianmu Mountain (Fig. 2). According to our previous studies, the germplasms of C. officinalis collected from the above three regions (Xixia in Henan, Foping in Shaanxi, and Lin’an in Zhejiang) have the best quality as well as largest quantity (Cao et al., 2016; Li et al., 2012; Bai et al., 2009). The total production of C. officinalis from the three main producing regions (Shaanxi, Henan and Zhejiang) accounts for 90 % of the total market in China (Bai et al., 2016; Li et al., 2012). Nevertheless, the yield of C. officinalis products cannot meet the rapidly growing market demand of pharmaceutical industry in recent years (Fig. 1). Therefore, convenient and effective strategies (specifically at environmental level) are needed to improve the yield of products for C. officinalis.

Introducing the medicinal crops from main producing regions to potential distribution regions is a good way to improve the yield of products (Verma et al., 2021; Testa et al., 2014). With the rapid development of China's transportation network, local governments attach great importance to the development of regional industry of Chinese medicine and the plantation technology of medicinal crops. In this situation, the cross-regional introduction of Chinese medicinal materials is becoming easier and more frequent in recent years. For C. officinalis, it is crucial to investigate whether the change of habitat affect the quality and efficacy of Chinese medicinal materials. In particular, it is necessary to investigate the contents of medicinal bioactive products and their formation mechanism. Thus, the question should be highly focused on how the medicinal bioactive products in Chinese medicinal materials change after the introduction from original habitat to new habitat with different environmental conditions.

Based on the above questions, we used C. officinalis as model plants to study the effects of environmental shifts on the functional traits and bioactive products of medicinal crops. In this study, six key environmental factors in original regions (ORs) and introduced region (IR) were recorded and comparatively analyzed. Seven fruit and seed functional traits of C. officinalis before and after introduction were estimated. The contents of seven main bioactive products of C. officinalis were measured using high performance liquid chromatography (HPLC) (Fig. 3). Further correlation analysis between the contents of bioactive products and environmental factors in different regions were conducted. Collectively, the aims of this study are: (1). to investigate the effects of environmental factors on the functional traits of C. officinalis; (2). to determine the effects of habitat shifts on the bioactive products of C. officinalis; (3). to reveal the correlations among functional traits, bioactive products and environmental factors; (4). to provide effective strategies for improving the yield of products of C. officinalis. Collectively, these results will help revealing the molecular mechanism of the formation of bioactive products in C. officinalis and providing references for investigating the effects of environmental shifts on the functional traits and bioactive products of medicinal crops under climate change.