OsSWEET11b, a sixth leaf blight susceptibility gene involved in sugar transport-dependent male fertility

Abstract

SummarySWEETs play important roles in intercellular sugar transport. Induction of SWEET sugar transporters by transcription activator-like effectors (TALe) of Xanthomonas ssp. is a key factor for bacterial leaf blight (BLB) infection of rice, cassava and cotton. Here, we identified the so far unknown OsSWEET11b with roles in male fertility and BLB susceptibility in rice. While single ossweet11a or b mutants were fertile, double mutants were sterile. Since clade III SWEETs can transport gibberellin (GA), a key hormone for rice spikelet fertility, sterility and BLB susceptibility might be explained by GA transport deficiencies. However, in contrast to the Arabidopsis homologs, OsSWEET11b did not mediate detectable GA transport. Fertility and susceptibility must therefore depend on SWEET11b-mediated sucrose transport. Ectopic induction of OsSWEET11b by designer TALe enables TALe-free Xanthomonas oryzae pv. oryzae (Xoo) to cause disease, identifying OsSWEET11b as a BLB susceptibility gene and demonstrating that the induction of host sucrose uniporter activity is key to virulence of Xoo. Notably, only three of now six clade III SWEETs are targeted by known Xoo strains from Asia and Africa. The identification of OsSWEET11b has relevance in the context of fertility and for protecting rice against emerging Xoo strains that evolve TALes to exploit OsSWEET11b.

SWEET13 transport of sucrose, but not gibberellin, restores male fertility in Arabidopsis sweet13;14

“…Recently, we discovered that Clade 3 SWEET members are involved in sugar transport-dependent male fertility in rice (14). OsSWEET11a and 11b accumulated in complementary sections of the vasculature of filament and anther, respectively (14).…”

“…Recently, we discovered that Clade 3 SWEET members are involved in sugar transport-dependent male fertility in rice (14). OsSWEET11a and 11b accumulated in complementary sections of the vasculature of filament and anther, respectively (14). In contrast, SWEET13 and 14 promoter-GUS reporter fusions did not appear active in the vasculature, but were in non-vascular tissues of the anther (12).…”

Sucrose rather than GA transported by AtSWEET13 and AtSWEET14 supports pollen fitness at late anther development stages

“…In 2016, Kanno and co-authors reported that AtSWEET10, AtSWEET12, AtSWEET13 and AtSWEET14 were able to mediate GA transport using a modified yeast two-hybrid system containing BD-GID1a (GA receptor) and AD-GAI (a DELLA protein). The same system has been used to detect weak GA transport activity for OsSWEET3a, OsSWEET11a and OsSWEET12 (Kanno et al ., 2016; Morii et al ., 2020; Wu et al ., 2022). However, the biological relevance of GA transport mediated by SWEETs was only indicated by partial restoration of anther dehiscence of the atsweet13;14 mutant through exogenous GA3 application (Kanno et al ., 2016), and restoration of defects in germination and early shoot development for ossweet3a (Morii et al ., 2020).…”

“…In rice, OsSUC1 is highly expressed in the wall of anther, and the ossucl mutant shows impaired pollen function without affecting pollen maturation (Hirose et al ., 2010). OsSWEET11a and OsSWEET11b are expressed in anther veins, and ossweet11a;11b mutant is male sterile (Wu et al ., 2022). In cucumber, the knockdown mutant of tapetum- and pollen-localized CsSUT1 shows male sterility (Sun et al ., 2019).…”

“…However, it is uncertain whether this rescue is due to altered GA transport or due to an indirect effect of GA on sugar transport because GA and sugar are interconnected in signaling pathways of many developmental processes, including flowering (Matsoukas, 2014). To clarify which substrate of AtSWEET13 and AtSWEET14 is important in anther to support pollen development, we used AtSWEET9, with sucrose transport activity but does not have GA transport activity (Lin et al ., 2014; Kanno et al ., 2016; Wu et al ., 2022), as a genetic tool to complement atsweet13;14 under control of the AtSWEET14 promoter. As a result, AtSWEET9 was able to fully rescue the defected pollen germination phenotype of atsweet13;14 .…”