Brassinosteroids regulate outer ovule integument growth in part via the control of INNER NO OUTER by BRASSINOZOLE‐RESISTANT family transcription factors

Abstract

Brassinosteroids (BRs) play important roles in regulating plant reproductive processes. BR signaling or BR biosynthesis null mutants do not produce seeds under natural conditions, but the molecular mechanism underlying this infertility is poorly understood. In this study, we report that outer integument growth and embryo sac development were impaired in the ovules of the Arabidopsis thaliana BR receptor null mutant bri1‐116. Gene expression and RNA‐seq analyses showed that the expression of INNER NO OUTER (INO), an essential regulator of outer integument growth, was significantly reduced in the bri1‐116 mutant. Increased INO expression due to overexpression or increased transcriptional activity of BRASSINAZOLE‐RESISTANT 1 (BZR1) in the mutant alleviated the outer integument growth defect in bri1‐116 ovules, suggesting that BRs regulate outer integument growth partially via BZR1‐mediated transcriptional regulation of INO. Meanwhile, INO expression in bzr‐h, a null mutant for all BZR1 family genes, was barely detectable; and the outer integument of bzr‐h ovules had much more severe growth defects than those of the bri1‐116 mutant. Together, our findings establish a new role for BRs in regulating ovule development and suggest that BZR1 family transcription factors might regulate outer integument growth through both BRI1‐dependent and BRI1‐independent pathways.

On the Way to Ovules: The Hormonal Regulation of Ovule Development

“…This phenotype, which was also found in BR mutants det2-1 and bri1-5, was due to a reduction in both cell length and number. Moreover, the bzr1-1D mutation was able to partially restore bri1-116 defects in outer integument growth (Jia et al, 2020), suggesting that BZR1 mediates the BRI1 outer integument growth regulation. According to this, in the sextuple null mutant of the six BZRs encoded in Arabidopsis, bzr-h, outer integument growth was completely arrested after initiation.…”

“…According to this, in the sextuple null mutant of the six BZRs encoded in Arabidopsis, bzr-h, outer integument growth was completely arrested after initiation. Moreover, both BRI1 and BZR1 were broadly localized in all ovule tissues from stage 2-I to stage 3-V, including the initiated and out-growing outer integument cells (Jia et al, 2020). Interestingly, using RNA-seq transcriptomic analysis, Jia et al (2020) found that INO, which regulates outer integument development (Villanueva et al, 1999), is upregulated in the ovules of bri1-116 bzr1-1D when compared with bri1-116.…”

“…Moreover, both BRI1 and BZR1 were broadly localized in all ovule tissues from stage 2-I to stage 3-V, including the initiated and out-growing outer integument cells (Jia et al, 2020). Interestingly, using RNA-seq transcriptomic analysis, Jia et al (2020) found that INO, which regulates outer integument development (Villanueva et al, 1999), is upregulated in the ovules of bri1-116 bzr1-1D when compared with bri1-116. Similarly, INO expression is repressed in bri1-116 but its expression is restored to a wild type level in the bri1-116 bzr1-1D double mutant (Jia et al, 2020).…”

“…For instance, the loss-of-function mutants bri1-5 (Huang et al, 2013), bri1-116 (Jia et al, 2020), and the gain-of-function mutant bin2-1 of the BR signaling negative regulator BRASSINOSTEROID-INSENSITIVE 2 (BIN2) (Huang et al, 2013;Jia et al, 2020), have fewer ovules and seeds than wild-type plants. On the contrary, the gain-of-function mutant bzr1-1D of the positive BR signaling regulator BRASSINAZOLE RESISTANT 1 (BRZ1) presents increased ovule and seed number (Huang et al, 2013;Barro-Trastoy et al, 2020).…”

“…However, it has not been until recently that BRs have been clearly implicated in the development of the integuments. Jia et al (2020) observed that in the bri1-116 mutant, defective in BR perception, around 21% of the ovules had a severe outer integument growth arrest, in which the outer integument was not able to surround the inner integument. This phenotype, which was also found in BR mutants det2-1 and bri1-5, was due to a reduction in both cell length and number.…”