Stepwise changes in flavonoids in spores/pollen contributed to terrestrial adaptation of plants

Protecting haploid pollen and spores against UV-B light and high temperature, 2 major stresses inherent to the terrestrial environment, is critical for plant reproduction and dispersal. Here, we show flavonoids play an indispensable role in this process. First, we identified the flavanone naringenin, which serves to defend against UV-B damage, in the sporopollenin wall of all vascular plants tested. Second, we found that flavonols are present in the spore/pollen protoplasm of all euphyllophyte plants tested and that these flavonols scavenge reactive oxygen species to protect against environmental stresses, particularly heat. Genetic and biochemical analyses showed that these flavonoids are sequentially synthesized in both the tapetum and microspores during pollen ontogeny in Arabidopsis (Arabidopsis thaliana). We show that stepwise increases in the complexity of flavonoids in spores/pollen during plant evolution mirror their progressive adaptation to terrestrial environments. The close relationship between flavonoid complexity and phylogeny and its strong association with pollen survival phenotypes suggest that flavonoids played a central role in the progression of plants from aquatic environments into progressively dry land habitats. Stepwise changes in spores/pollen flavonoids promote spores/pollen adaptation in the terrestrial environment by absorbing UV-B and eliminating Reactive oxygen species.

Automated summary

Protecting haploid pollen and spores against UV-B light and high temperature is critical for plant reproduction and dispersal. Flavonoids, such as naringenin and flavonols, play an important role in this process by defending against UV-B damage and scavenging reactive oxygen species. The synthesis of flavonoids in pollen during ontogeny and their complexity progressively increasing during plant evolution suggest their central role in the adaptation of plants from aquatic to terrestrial environments.