Partial Shade Balances Sucrose-Starch Metabolism via
Compensation by PF Leaves
Plants are autotrophic organisms, and sugar metabolism in plants
represents their growth regulation, stress tolerance response, and
productivity. Therefore, monitoring carbohydrate status and metabolic
activities in plants could be crucial for estimating the influence of
various light conditions on the production and allocation of
photoassimilates. The two most important carbohydrate pools that result
from carbon assimilation during photosynthesis include the storage pool
(starch) and export pool (sucrose). Sucrose, an important output of
photosynthesis, is synthesized by the sucrose phosphate synthase (SPS).
In contrast, sucrose synthase (SS) is involved in catalysis, both the
degradation and synthesis of sucrose in plants
(Du et al., 2020). Similarly, starch is
the main storage carbohydrate in plants. Its metabolism through amylases
(α and β) and debranching enzymes (DBEI, DBEIIa, and DBEIIb) are crucial
for stress response and sugar biosynthesis under stress conditions
(Du et al., 2020;
Stitt & Zeeman, 2012;
Streb & Zeeman, 2012). Previously,
researchers reported the increased transportation and starvation of
sugar under environmental stress that promotes plant growth and enhances
stress capacity (Lemoine et al., 2013;
Paparelli et al., 2013). Our
investigations demonstrated that partial light conditions (PL) enhanced
the soluble sugar and sucrose levels than normal light conditions (NL)
(Fig. 4). We speculated the mutual balancing and compensation of sugar
levels between the two sides of leaves (PF and PS) under partial light
conditions, which might be a reason for delayed leaf senescence under PL
conditions. It has been extensively reported that starch is hydrolyzed
into sugar in response to stress (Amiard et
al., 2005; Burke, 2007;
Thalmann et al., 2016). Similarly,
partial shading (PS) significantly induced starch degrading enzymes
during the first ten days after flowering. This decline in soluble
starch content and sucrose synthase activity in PL leaves triggered the
sucrose synthesis in PF leaves and its transport towards PS leaves to
compensate for the initial breakdown of starch. Furthermore, light
receptor PHYB has been reported to promote starch accumulation
(Han et al., 2017;
Sun et al., 2017). Consistent with these
reports, our idea showed that the increased expression of ZmPHYB1c in PF
enhanced starch and sugar biosynthesis through starch degradation in PF,
which compensated PS leaves. This mechanism helped maintain leaf
greenness in maize under partial shading
(Li et al., 2020). It probably created a
synergy between the two side leaves that increased SPS and SS activity
in PF leaves to maintain the sucrose and starch content in PS leaves,
which helped in delaying senescence. On the other hand, the decrease in
photosynthetic rate preceded leaf yellowing under all conditions, which
might have induced leaf senescence through decreased sugar levels
(Quirino et al., 2000). Similar results
were reported in a previous report in which sugar degradation in
complete shading resulted in leaf yellowing and increased relative
electrolyte leakage (van Doorn, 2008).
Subsequently, we traced the translocation through the carbon labeling to
verify the regulation of sugar synthesis between PF and PS, and the
distribution of photoassimilates under partial and normal light
conditions. A significant increase of 13C abundance in
the leaves of partial shading rather than normal light in day 1 to day
10 indicated the higher sugar production under PL (Fig. 4). A similar
situation for a maximum peak of 13C was observed in
ryegrass shoot day 1 (Butler et al.,
2004). In addition, 13C abundance in different parts
of the maize plant was significantly elevated in the middle and bottom
leaves in PL at day 1 under partial shading
(Peuke et al., 2001). Combined with the
evidence from increased Pn (Table 2),
up-regulated and higher contribution of soluble sugar and sucrose
synthesis by PF than PS (Fig. 3A, C-E) and, the higher13C abundance in the stem during initial ten days and
then in-ear during late 30 days (Fig. 4) under PL inferred that partial
shade enhanced the photosynthetic carbon fixation function of PF leaves.
Furthermore, we confirmed that about 5% of 13C was
transferred from PF into PS, and 70% of the 13C was
supplied to the middle and lower leaves when the ear was not fully
formed after flowering. It is shown that an increase in sugar level and
balance of sugar transfer between the PF and PS leaves helped the leaves
to maintain greenness under a partial light environment.
To further verify this hypothesis at the molecular level, we analyzed
the expression pattern of sugar transporter genes, i. e., SUT, that help
to diffuse sucrose into phloem through the apoplast pathway
(Riesmeier et al., 1992;
Sauer, 2007). Another essential sucrose
transporter, “SWEET”, transfers the sucrose from parenchyma to
apoplast (Chen et al., 2012). Keeping in
view the role of SUT and SWEET genes in sucrose transport, we observed
the expression pattern of ZmSUT1a and ZmSWEET11.1 under
normal and partial light conditions. In line with our speculation and
pre-mentioned results, both genes (ZmSUT1a andZmSWEET11.1) showed significantly higher expression under the PL
than NL conditions. Interestingly, the ZmSUT1a andZmSWEET11.1 were up-regulated considerably during the first ten
days in PF leaves. However, from day 25th and onward,
the two genes showed significantly higher expression in PS leaves,
indicating that sugar transport was increased towards the PS leaves.
Overall, it verifies our hypothesis about the balancing of sugar in PS
leaves by PF leaves under shading conditions that could delay senescence
in both side leaves, which increases the outflow of sugar into the ear,
as seen from the delayed grain filling period (Fig. 4D, 6C, 8). We
suggest that partial shade stimulation may have enhanced the
photosynthetic carbon sequestration function of PF leaves to compensate
for the carbon assimilation in PS leaves and improved carbon balance and
resistance on both sides. Altogether, these results suggested an
increase in sugar levels and sugar balance between PF and PS was
required for the delayed leaf senescence in maize.