Boron (B) is a metalloid and a beneficial element for maintaining the structural integrity of cell walls, which can reduce the uptake and accumulation of harmful substances in crops, thereby alleviating physiological damage caused by abiotic stresses (Qin et al., 2021; Qin et al., 2022; Yan et al., 2022). Negative alterations in these aforementioned physiological processes lead to a significant reduction in leaf area as well as biomass, retarded plant growth, and declined yield quality (Wang et al., 2015; Wei et al., 2022). Boron deficiency in soils is a widespread problem in agricultural production. Currently, B deficiency has led to reductions in yields of 132 crops in over 80 countries (Latifi and Jalali, 2018; García-Sánchez et al., 2020). Moreover, the exogenous application of B was reported to enhance dry matter synthesis and accumulation, which leads to an increase in crop yield (Zhou et al., 2013; Ahmed et al., 2020). Additionally, B plays a vital role in photosynthesis and transportation of the photoassimilates (Sharma and Ramchandra, 1990; Mishra et al., 2018). Boron deficiency is known to cause the impairment of leaf structure and function of the plant, resulting in reduced photosynthetic pigment content, reduced CO₂ assimilation rate, and modulated blade expansion (Mukhopadhyay et al., 2013; Cong et al., 2015).

The cultivated land in China has a deficiency of B spreading across 33 million hectares. Sugar beet is an economic crop in northern China with a high B requirement. Low B-containing soils inevitably affect yield and sugar content, leading to lower economic returns from sugar beet cultivation and seriously limiting the development of the sugar industry in China. Different crop genotypes vary in their B requirements and utilization capacity (Pommerrenig et al., 2018). Employing B-efficient crops can effectively ameliorate the environmental risks associated with B administration and may help to promote sustainable agricultural development. Earlier studies on screening B-efficient grape cultivars (Vitis vinifera L.) have been reported as early as 1941 (Scott, 1941). Currently, the identification of B-efficient genotypes, with in-depth knowledge of physiological and molecular mechanisms, has been widely carried out in plants such as cotton (Gossypium spp) (Wu et al., 2018), oilseed rape (Brassica napus L.) (Yang et al., 2013), citrus (Citrus sinensis Obs) (Liu et al., 2017) and other horticultural crops.

In previous studies, 57 sugar beet cultivars grown worldwide for B utilization efficiency were identified (Song et al., 2021a; Wu et al., 2021; Song et al., 2022), and have obtained sugar beet B-efficient cultivars. Nevertheless, it is still unclear whether the physiological traits of B-efficient sugar beet cultivars correlate with leaf photosynthetic parameters under B-deficient conditions. The study investigated the changes and associations of leaf growth parameters, chloroplast ultrastructure, photosynthetic rate, and chlorophyll fluorescence (ChlF) parameters in sugar beet cultivars differing in B-efficiency under B deficit. Moreover, the study demonstrated how B-efficient cultivars responded to B stress, leading to changes in the leaf morphology, structure, and photochemical efficiency in different cultivars. This study will provide a theoretical basis for the utilization of B-efficient sugar beet cultivars in future breeding programmes.

In current study, the KWS1197 cultivar was more advantageous in terms of leaf phenotypic traits, photosynthetic performance, and energy utilization of the PSII ( Figure 8 ). Boron deficiency caused increased LMR and insignificant SBR changes in the two tested sugar beet cultivars, ultimately leading to an improved ratio of assimilated to non-assimilated tissues and a reduced plant growth rate. Compared to the KWS0143 cultivar, the higher growth rate of the KWS1197 seedlings suggest that this sugar beet cultivar’s foliage had a greater adaptive response to the B-deficient environment. It has also been shown that B-deficient growth conditions significantly reduced biomass in Sacha inchi and Neolamarckia cadamba (Yamuangmorn et al., 2021; Yin et al., 2022). Furthermore, a study conducted on citrus plants demonstrated that B-efficient genotypes experienced less reduction in biomass under low B conditions (Liu et al., 2015). Contrastingly, in a study based on B-inefficient genotype of Arabidopsis, the growth rate was significantly reduced, and growth/development was significantly delayed under B deprivation (Pommerrenig et al., 2018), which remains consistent with the present findings. Furthermore, it was revealed that B-deficiency stress significantly impacted the P_n of different sugar beet cultivar seedlings. However, the KWS1197 cultivar underwent lesser reduction and exhibited a rather greater net photosynthetic rate than the B-inefficient variety. Similarly, B deprivation was found to cause a decrease in P_n in cabbage and cotton plants by means of Hill reaction’s inhibition and a decrease in C_i (Choi et al., 2016). Previous studies have shown that B deficiency decreased gas exchange parameters in grapes, but the decrease was also smaller in B-efficient genotyped grape cultivars (Wei et al., 2022).

Some studies have found that B-deficient environments also affect photosynthetic pigments’ content. For example, B deficiency was found to reduce chlorophyll content in studies on citrus (Hua et al., 2017; Yan et al., 2022). Albeit, other studies have found an increase in chlorophyll content after short-term low B treatment (Chen et al., 2014). Conversely, a study on cotton found that chlorophyll content changed unremarkably when B-deficient stress reduced the P_n of leaves (Liu et al., 2017). The current study found that under B-deficient conditions, the amount of photosynthetic pigment did not change significantly. It might be because the duration of B-deficient treatment and the degree of B-deficient stress were associated, indicating that the change in photosynthetic pigment content in this study was not the dominant factor causing the decline in leaf photosynthetic rate. On the other hand, the effect of B deprivation on the photosynthetic performance of plants was also reflected in the damage to photosynthetic organs. In citrus studies, it was revealed that chloroplast structure was also damaged in B-deficient stress, leading to reduced CO₂ assimilation (Yan et al., 2022), and thus affecting photosynthetic rate (Yang et al., 2022). The present investigation established that grana were disorganized and structurally abnormal under B deficiency. Notably, compared to the KWS0143 cultivar, KWS1197 showed a complete chloroplast structure and neatly arranged lamellar structure of leaves.

It has been demonstrated earlier that B deficiency does not directly damage the PSII and impact photosynthesis, but rather the photoinhibition caused by B deficiency is associated with abnormal carbon metabolism (Han et al., 2008). The adverse effects of B deprivation on the photosynthetic system can be reflected by PSII, which eventually causes alterations in fluorescence. The current study showed that the positive ΔK-band indicated OEC deactivation, fewer antenna complex connections, and a distorted thylakoid membrane. Furthermore, it ultimately led to reduced energy transfer and uptake efficiency, which was also observed in studies of nitrogen-deficient as well as calcium-deficient crops (Aleksandrov et al., 2014; Cetner et al., 2017). Additionally, with B deficiency stress, the ABS/RC increased while ET_o/RC and ET_o/CS_m decreased; the DI_o/RC and DI_o/CS_m tended to increase, indicating that B deficiency increased the light energy absorbed while decreasing the energy used for electron transfer in sugar beet seedling leaves, which is consistent with the appearance of a positive ΔK-band. While the dissipated energy increased (DI_o/RC and DI_o/CS_m ), which in turn could reduce the excess excitation energy (ABS/RC) in PSII and positively protect the integrity of the electron transport chain. The KWS1197 cultivar’s photochemical efficiency was higher than the KWS0143. In citrus, light energy absorbed also increased because of B deficiency, which implies a partial inactivation of the reaction center (Han et al., 2009) and an increase in the energy dissipated to avoid photo-oxidative damage (Aleksandrov et al., 2014), a mechanism to protect damaged leaves. The same conclusion has been drawn in studies on Lolium Perenne L. (Zhang et al., 2018).

The leading site of impaired electron transport is the inactivation of the PSII receptor side, which indicates the occurrence of photo-inhibition damage (Ye et al., 2019). During B-deficient stress, ΔJ-band and ΔI-band appeared in different cultivars of sugar beet leaves, indicating that B deprivation affected the reduction of the PSII receptor side and oxidation of the PSI receptor side, resulting in the photo-inhibition. It became apparent that φ_Eo, φ_Ro decreased in B deficiency ( Figure 6B ), demonstrating photochemical reactions on PSII for electron capture as well as transfer. The reduced efficiency of the photochemical reaction on PSII for electron capture and transfer, together with the reduced PI_abs , reflects the impaired reduction of the terminal electron acceptors of PSI in sugar beet. The magnitude of change was less in the KWS1197 cultivar than the KWS0143. It was found in studies involving tomato seedlings that the light energy absorbed by the leaf PSII reaction center increased in the presence of reduced RE_o/CS_m (Kalaji et al., 2014). The same finding was established in the present study, which could be a protective mechanism for sugar beet seedlings to enable energy availability under B deficiency.

The current study alluded that B deficiency retarded leaf growth and development of contrasting B efficiency sugar beet cultivars, reducing the photosynthetic rate and photochemical efficiency of the PSII. Meanwhile, inactivation of the PSII receptor side induced the onset of photoinhibition, limiting light energy transfer, and thus reducing the CO₂ assimilation rate of sugar beet. The KWS1197 cultivar of sugar beet leaves in comparison with the KWS0143 cultivar under B deficient growth conditions had less reduction in P_n . Meanwhile, the KWS1197 cultivar was suggested to have an accumulation of biomass, a better intact structure of thylakoid, higher energy transfer and absorption efficiency in PSII, a stronger activity of OEC and reaction center, higher light utilization efficiency, and was exposed to a less degree of photoinhibition. The advantage of the KWS1197 cultivar in photochemical utilization under B deficiency is one of the critical reasons for the difference under B efficient conditions, which enriches the theoretical basis for the effective use of B nutrition in sugar beet. The present study will help the breeders understand and select the B-efficient cultivars of sugar beet by screening photosynthetic parameters, which were shown to correlate with biomass and yield parameters.

The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding authors.

XS: Writing-review and editing. Investigation, Software. BS: Conceived and designed the experiments, Supervision and Funding acquisition. JH: Software and Writing review & editing. MFA and QJ and WW and WH: Writing-review & editing. HL and BS and AK and WH: Writing-review & editing and Funding acquisition All authors contributed to the article and approved the submitted version.