Longfei Wang, Shuai Cao, Peitong Wang, Kening Lu, Qingxin Song, Fang-Jie Zhao, and Z. Jeffrey Chen

PNAS March 30, 2021 118 (13) e2023981118

Significance

Polyploidy can stimulate genetic and epigenetic changes that enhance the potential for plant adaptation and fitness under extreme environments, but the molecular basis for this is poorly understood. Here we show that tetraploid rice is more tolerant to salinity than diploid rice. Tetraploidy induces DNA hypomethylation which potentiates genomic loci coexistent with stress-responsive genes including those in jasmonate biosynthesis and signaling pathways for rapid and robust responses under stress. After salt stress, elevated expression of salt-responsive genes can induce hypermethylation and suppress adjacent TEs. This feedback regulation between polyploidy-induced DNA hypomethylation in rapid and strong stress response and stress-induced hypermethylation to repress TEs and/or TE-associated genes may provide evolutionary advantages for selection to enhance adaptation in polyploid plants and crops.

Abstract

Polyploidy is a prominent feature for genome evolution in many animals and all flowering plants. Plant polyploids often show enhanced fitness in diverse and extreme environments, but the molecular basis for this remains elusive. Soil salinity presents challenges for many plants including agricultural crops. Here we report that salt tolerance is enhanced in tetraploid rice through lower sodium uptake and correlates with epigenetic regulation of jasmonic acid (JA)–related genes. Polyploidy induces DNA hypomethylation and potentiates genomic loci coexistent with many stress-responsive genes, which are generally associated with proximal transposable elements (TEs). Under salt stress, the stress-responsive genes including those in the JA pathway are more rapidly induced and expressed at higher levels in tetraploid than in diploid rice, which is concurrent with increased jasmonoyl isoleucine (JA-Ile) content and JA signaling to confer stress tolerance. After stress, elevated expression of stress-responsive genes in tetraploid rice can induce hypermethylation and suppression of the TEs adjacent to stress-responsive genes. These induced responses are reproducible in a recurring round of salt stress and shared between two japonica tetraploid rice lines. The data collectively suggest a feedback relationship between polyploidy-induced hypomethylation in rapid and strong stress response and stress-induced hypermethylation to repress proximal TEs and/or TE-associated stress-responsive genes. This feedback regulation may provide a molecular basis for selection to enhance adaptation of polyploid plants and crops during evolution and domestication.

See: https://www.pnas.org/content/118/13/e2023981118

Figure 1:

Enhanced salinity tolerance in 02428 tetraploid rice. (A) Morphological changes in diploid (2×) and tetraploid (4×) rice in response to saline treatments (0 and 125 mM NaCl) for 6 d followed by recovery in water for 5 d. (Scale bar = 5 cm.) (B) Survival rates of diploid and tetraploid rice (n = 6 biological replicates, each replicate with 32 plants). (C) Inhibition rates of diploid and tetraploid rice after salt stress. Seedlings at trefoil stage were treated with 125 mM NaCl for 1 to 5 d. Dry weight of roots was used to calculate inhibition rates (n = 18 biological replicates, each replicate with 2 plants). (D) Sodium content in roots under the saline condition for 2 and 4 d (n = 12 biological replicates, each replicate with 2 plants). Single and double asterisks indicate statistical significance of P < 0.05 and P < 0.01, respectively (Student’s t test).