In the present study, a panel of 123 hemp accessions was used to study the variability in hemp fiber quality and to enlighten key components of this variability. The analysis of the hemp panel revealed extensive variation in 28 fiber quality-related traits among the hemp accessions. In addition, some accessions displayed characteristics that are highly appreciated by the hemp industry. Such traits included large contents of bast fiber and cellulose, low contents of lignin and pectin, fine fiber bundles (high P_L and P_H values), and late flowering time (Ranalli, 2004; Salentijn et al., 2015). Accessions IWRNZ-902 and WU-111 exhibited several of these phenotypes and thus have a considerably higher quality fiber compared to many other accessions. These accessions indicate valuable germplasm to include in breeding programs, aiming to improve hemp fiber quality.

We observed that important fiber quality traits have a large fraction of heritable phenotypic variation, as indicated by the large G% and H². As in the present study, extensive genetic studies have shown large heritability values for cell wall components (cellulose, hemicellulose, and lignin) in other fiber crops, such as poplar and eucalyptus (Raymond and Schimleck, 2002; Klasnja et al., 2003; Schimleck et al., 2004; Poke et al., 2006; Davis, 2008), miscanthus (Slavov et al., 2014; Van Der Weijde et al., 2017), switchgrass (Mclaughlin et al., 2006; Boe and Lee, 2007), and maize (Torres et al., 2015). Furthermore, similar heritability values for flowering time were reported in several plant species such as almond [reviewed in Sánchez-Pérez et al. (2014)], apricot (Campoy et al., 2011), arabidopsis (Sasaki et al., 2015), cotton (Kushanov et al., 2017), flax (Soto-Cerda et al., 2014; You et al., 2017), and rice (Takahashi et al., 2001; Huang et al., 2010). It seems plausible that a large fraction of the phenotypic variation of biomass and flowering traits might be controlled by highly “robust genetic systems,” although they are highly complex and polygenic traits, since respectively ~4,000 (Wang et al., 2012) and ~300 genes are estimated to be involved in cell wall synthesis and flowering in arabidopsis (Wang et al., 2012; Bouché et al., 2016). The robust genetic systems might work to control the performance of these traits so that they are less sensitive to environmental differences. This guarantees important functions such as fiber production and reproduction regardless of the environment.

The crucial functions of these traits might support such high heritability values controlled by robust genetic mechanisms. From an evolution point of view, the cell wall performs a structural function in shaping the cells and consequently to plant bodies (Sarkar et al., 2009). Particularly, cellulose and lignin can withstand mechanical pressure exerted by the gravitational pull and the load of the plant body, providing mechanical strength to the plant (Volkmann and Baluška, 2006). In addition, lignin provides protection functions against UV radiation and against pathogens, such as microbes, fungi, and animals, that allowed plants to conquer terrestrial habitats (Iiyama et al., 1994; Popper et al., 2011). Hemicellulosic polysaccharides also provide structural rigidity to the cell walls (Pauly et al., 2013). Hemicellulose and lignin create a matrix around microfibrils of cellulose affecting the recalcitrance of the cell walls (Torres et al., 2015). Furthermore, flowering is an essential biological process for many plants as the survival of the species depends on it (Mouradov et al., 2002). Consequently, these biomass and flowering traits seem to perform essential roles that cannot be widely modified, as the consequences might be lethal for the plant.

Furthermore, we observed that hemp fiber quality-related traits are not strongly stable across environments, as indicated by the significance of G×E interaction components. The results showed that some accessions were more sensitive in some environments than in others. It seems likely that the phenotypic variation associated to the G×E interactions might be controlled by “plastic genetic systems” where certain genes are expressed when combined with specific environmental conditions. This is the first study describing significant G×E interactions in fiber and flowering traits in hemp. Studying these interactions is important owing to their implications for the setup of selection experiments, as the ranking of accessions is dependent on the environment (Van Der Weijde et al., 2017). Selection for traits with large G×E interactions in breeding programs might lead to biased selection decisions, owing to the unknown effects in untested environments. Nonetheless, the G×E interactions were small in most important cell wall components (contents of glucose, mannose, xylose, ADL, and KL), fiber content, and flowering traits in hemp. Similar small G×E interactions have been shown for biomass traits, especially contents of cellulose, hemicellulose, and lignin, in several fiber crops, such as alfalfa (Sheaffer et al., 1998), maize (Dolstra et al., 1992; Cox et al., 1994; Argillier et al., 1997; Barrière et al., 2008; Torres et al., 2015), miscanthus (Van Der Weijde et al., 2017), and switchgrass (Hopkins et al., 1995). Therefore, the extent of the G×E interaction effects on these fiber quality-related traits might not strongly affect the ordering of hemp accessions across environments and might not interfere in selection decisions.

Interesting examples of large G×E interactions in hemp are the contents of some pectin-related monosaccharides. The evolution and the functions of pectin in plants might explain these results. In the stem of plants, pectins are mostly present in the middle lamella between cells and are involved in the intracellular adhesion, providing integrity and rigidity to plant tissues and to the stem. They also play important roles in the defence mechanisms against pathogens. In addition, they are involved in the regulation of the ion transport and in the water holding capacity (Voragen et al., 2009). Yet, pectic polysaccharides are highly dynamic structures, and their content dramatically changes across tissues and plant species (Willats et al., 2001). Pectin has almost disappeared in the stems from several modern plants, such as grasses (Carpita and Gibeaut, 1993; Carpita, 1996; Sarkar et al., 2009; Voragen et al., 2009), suggesting that their important functions might be evolutionary replaced by other cell wall components. Lignin is the newest cell wall component to appear in plants and has some parallel functions with pectin, such as structural support and defence functions (Sarkar et al., 2009). As a consequence, dramatic changes of pectin content might not be lethal to plants, owing to a putative partial compensation from other cell wall components, which might allow larger plasticity in sensitivity of certain accessions in different environments.

Fiber quality-related traits were strongly influenced by the differences of the environments across the trial locations. Previous studies have reported large sensitivity of hemp to the environment, particularly to the photoperiod and temperature regimes, affecting the vegetative growth and flowering of the plants (Faux et al., 2013; Amaducci et al., 2015; Sawler et al., 2015). This large sensitivity can be understood as a strong general response of hemp accessions to adapt to the environment, independently of the heritable genetic control of the traits described in previous paragraphs. This behavior might be the result of the optimization of the plant fitness under specific environmental conditions. Consequently, the environment of the growing locations should be taken into account when selecting the cultivation purpose of hemp, and subsequent breeding should be done for use in a specific environment.

An example of the adaptive behavior of hemp is the difference in biomass production and flowering time across environments. Plants of the same accession grown in the Netherlands produced larger biomass and flowered later than plants grown in the other two locations. These variations can be explained by differences in photoperiod regimes across locations. Hemp is a short-day plant, and the length of the vegetative growth period depends on the shift from long- to short-day photoperiod regimes (Amaducci et al., 2012). The vegetative growth period is characterized by biomass production, after which this behavior shifts toward fiber maturation (secondary fiber formation and lignification) and plant reproduction during flowering development (Van Der Werf and Turunen, 2008; Liu et al., 2015). At northern latitudes, the shift from long-day toward short-day photoperiod regimes occurs later and therefore the critical photoperiod for flowering (~14–16 h) is reached later in the growing season of hemp (Struik et al., 2000; Hall et al., 2012). As a result, the cultivation of hemp focused on the production of fibers may be better in northern latitudes, while the cultivation of hemp for seeds or dual purpose seed/fiber in southern latitudes may be more adapted to the environment (Amaducci et al., 2015). The selection of the cultivation purposes based on the environment might increase the profitability of hemp cultivation, complementing the high fiber quality achieved by the breeding programs using the heritable phenotypic variation.

Another example of the adaptive behavior of hemp's biomass is the difference in production of monosaccharides composing pectin from plants across environments. Plants grown in France showed the largest content of monosaccharides composing pectin while plants of the same accessions in the Netherlands showed the lowest contents. It has been previously reported that pectin plays a role in modulating cell wall architecture in response to low availability of water [reviewed in Le Gall et al. (2015)], owing to its water holding capacity function (Voragen et al., 2009). As shown in Table 2, France had lower rainfall and larger days without rain than Netherlands. Based on the environmental differences between the locations and the functions of pectin, it seems plausible to hypothesize that hemp plants may increase the content of pectin in the stem partially as a response to the changes in water availability. This relationship may have important implications in the improvement of the fiber quality of hemp, as the contents of monosaccharides composing pectin are poorly heritable traits and pectin plays a key role in the fiber quality. Pectin has been associated to difficulties in decortication which results in increased fiber damage (Ranalli, 2004; Müssig et al., 2008; Salentijn et al., 2015) after fiber decortication. Furthermore, plants grown in Netherlands showed larger decortication efficiencies than in the other two locations, and the content of galacturonic acid, the main component of pectin (Willats et al., 2001), was positively correlated to the shive content after decortication (χ). These results indicate that lower contents of galacturonic acid in the stems results in easier decortication. In addition, it suggests that water availability may play a role in the pectin content, and if that is the case, it could be used as a tool to improve fiber quality associated to poor heritable traits. Crop management, such as irrigation, could contribute to the decrease in the pectin content and thus improve the quality. The present study provides interesting results to further investigate the influence of water availability on pectin content of hemp. The use of a wider range of locations with contrasting and more detailed environmental conditions and the use of controlled experiments may be useful to get insights into the role of specific environmental factors in hemp fiber quality.

Finally, the correlation analysis revealed that monoecious and dioecious plants have a different relationship with fiber quality. The results of the hemp panel analysis confirm that monoecious accessions have larger fiber qualities than dioecious. These differences may be explained by the larger uniformity in fiber production common in monoecious accessions compared to dioecious accessions (Mandolino and Carboni, 2004; Amaducci and Gusovius, 2010; Faux et al., 2013; Faux et al., 2014; Salentijn et al., 2015; Faux et al., 2016). Finally, the sex determination of hemp is another key element that should be taken into account when selecting the germplasm for breeding programs as it has important implications in fiber quality (Amaducci and Gusovius, 2010; Amaducci et al., 2015).