Stable expression of aquaporins and hypoxia-responsive genes in adventitious roots are linked to maintaining hydraulic conductance in tobacco (Nicotiana tabacum) exposed to root hypoxia

Abstract

Formation of adventitious roots in plants is a common response to hypoxia caused by flooding. In tobacco, after one week of root hypoxia treatment, plants produced twice as many adventitious roots as the aerated plants, but their maximum length was reduced. Hypoxia severely reduced net photosynthesis, transpiration rates, and photosynthetic light responses. Relative transcript abundance of the examined aquaporins in lateral roots was reduced by hypoxia, but in adventitious roots it remained unchanged. This apparent lack of an effect of root hypoxia on the aquaporin expression likely contributed to maintenance of high hydraulic conductance in adventitious roots. Lateral roots had lower porosity compared with adventitious roots and the expression of the ACS (1-aminocyclopropane-1-carboxylate synthase) gene was induced in hypoxic lateral roots, but not in adventitious roots, providing additional evidence that lateral roots were more affected by hypoxia compared with adventitious roots. ATP concentrations were markedly lower in both hypoxic lateral and adventitious roots compared with aerated roots, while the expression of fermentation-related genes, ADH1 (alcohol dehydrogenase 1) and PDC1 (pyruvate decarboxylase 1), was higher in lateral roots compared with adventitious roots. Since root porosity was greater in adventitious compared with lateral roots, the results suggest that the improved O2 delivery and stable root aquaporin expression in adventitious roots were likely the key factors helping flooded tobacco plants maintain high rates of root hydraulic conductance and, consequently, shoot gas exchange.

Identification of nitric oxide (NO)-responsive genes under hypoxia in tomato (Solanum lycopersicum L.) root

“…The latter study demonstrated that beside PIP1;3, PIP1;1 was also down-regulated after 2 days of hypoxia treatment. Moreover, down-regulation of other AQP encoding genes such as PIP1;2, PIP1;4, PIP2;1 in LR, was observed after one week of hypoxia treatment 99 . The authors did not observe any difference in hydraulic conductance (K r ) between hypoxic and aerated plants, indicating the efficiency of AR in root water transport in tobacco.…”

The State of the Art in Modeling Waterlogging Impacts on Plants: What Do We Know and What Do We Need to Know

“…Water absorption by roots is at least partially ( ~ 50%) governed by root water channels (aquaporins) of the plasma membrane intrinsic protein (PIP) family (McElrone et al, 2007; Tournaire‐Roux et al, 2003). The production of PIPs aquaporin‐like proteins differs between anaerobic and aerobic conditions among several soybean cultivars with varying degrees of waterlogging tolerance (Jitsuyama, 2017; Tan & Zwiazek, 2019). Incorporating this trait into crop models may help to account for genetic diversity for waterlogging tolerance under waterlogging conditions.…”

What Makes Adventitious Roots?

“…Beside constitutive AR, plants can produce AR in response to the environment: in response to anoxia stress provoked by flooding [36,37], to dark-light transitions such as a dark storage period condition for cuttings or light control of auxin homeostasis [38,39,40], to stem cutting [12,21,39,41] and to hormones [17,42]. Table 1 provides a non-exhaustive list of species for which adventitious roots are described in the present review.…”

“…In Arabidopsis, inhibition of growth of the main root system and the promotion of AR elongation under hypoxia restrict the root system in upper soil layers where the oxygen shortage may last for shorter time periods [36]. This is also supported by the observation of tobacco plants producing more AR in the hypoxia condition, but with reduced maximum length [37]. AR can contribute to flooding adaptation by taking up oxygen [38,55].…”

“…AR can contribute to flooding adaptation by taking up oxygen [38,55]. A greater AR porosity and stable root aquaporin expression suggest that AR are likely the key factors to maintaining high rates of root hydraulic conductance and shoot gas exchange in flooding conditions [37].…”