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Lateral root formation is a critical agronomic trait in plant architecture that determines crop productivity and environmental stress adaptability. It is therefore tightly regulated both by intrinsic developmental cues, such as abscisic acid (ABA) and auxin, and by diverse environmental growth conditions, including water deficit and high salinity in the soil. We have recently reported that an Arabidopsis R2R3-type MYB transcription factor, MYB96, regulates lateral root meristem activation under drought conditions via an ABA-auxin signaling crosstalk. In this signaling scheme, the MYB96-mediated ABA signals are incorporated into an auxin signaling pathway that involves a subset of GH3 gene encoding auxin-conjugating enzymes. The MYB96-overexpressing, activation tagging mutant, which is featured by having dwarfed growth and reduced lateral root formation, exhibits an enhanced drought resistance. In the mutant, expression of the GH3 genes was significantly elevated, which is consistent with the reduced lateral root formation. In contrast, the MYB96-deficient knockout mutant produced more lateral roots and was more susceptible to drought stress. Our observations strongly support that MYB96 is a molecular link that integrates ABA and auxin signals in modulating auxin homeostasis during lateral root development, particularly under water deficit conditions. It is also envisioned that the MYB96-mediated signals are related with pathogen resistance response, which is also profoundly affected by water content in plant cells.
The MYB transcription factors, consisting of approximately 170 members, comprise one of the largest transcription factor families in the Arabidopsis genome.1 They are classified into three subfamilies by the number of adjacent sequence repeats in the MYB domain. Approximately 70% of the MYB members have two imperfect repeats (R1 and R2), each repeat containing ~50 residues that form a helix-turn-helix configuration, belong to the R2R3-type subfamily in Arabidopsis.1,2 The R2R3-type MYB members regulate a wide array of plant developmental processes and plant responses to environmental stresses, such as anthocyanin accumulation,3 secondary metabolism,4 epidermal cell patterning5,6 and abiotic stress signaling.7–9
Numerous transcription factors have been found to mediate drought resistance responses. Transgenic or mutant plants with altered expression of such drought-inducible genes exhibit disturbed stomatal aperture and thus distressed response to water deficit conditions. However, only a few transcription factor genes have been shown to regulate root formation under drought conditions. It is therefore notable that the MYB96 transcription factor plays a role in lateral root growth under drought stress.
We have isolated an activation tagging mutant that constitutively overexpresses the MYB96 gene from a T-DNA insertional Arabidopsis mutant pool. The MYB96-overexpressing mutant exhibits an enhanced drought resistance with reduced lateral root density. While the primary root growth is unaffected in the mutant, the number of lateral roots is significantly reduced. Consistent with this phenotype, the MYB96 gene is expressed to a high level in the lateral root primordia. More careful examination revealed that reduced lateral root number in the mutant is caused by arrested activation of the lateral root meristem. In addition, while lateral root initiation and establishment of lateral root primordia are essentially normal, lateral root elongation is significantly suppressed. These phenotypes are also observed in plants treated with ABA or grown under osmotic stress.10,11 The previous and our own observations support that lateral root development is closely related with ABA and drought stress.
Whereas suppression of lateral root development is a well-known response to drought stress, not all of the mutants that are resistant to drought stress exhibit reduced lateral root number. For example, the enhanced drought tolerance 1 (edt1) mutant has an enhanced root system with longer primary root and more lateral roots.12 It is therefore likely that there are extensive signaling crosstalks in regulating root development under drought stress.
Our data support that the MYB96 gene plays inter-related but distinct in the shoots and roots under drought conditions. While ABA induces the MYB96 gene both in the shoots and roots, auxin induces the MYB96 gene primarily in the roots. Furthermore, MYB96 regulates different targets differentially in different organs: it regulates RD22 in the shoots but regulates primarily a subset of the GH3 genes in the roots in response to drought stress. Although ABA induction of the GH3 genes is unaffected in the shoots of the MYB96-deficient mutant (myb96-1), it is significantly diminished in the roots of the myb96-1 mutant in response to ABA. It is interesting that a transcription factor plays dual roles in different organs.
To look into the functional relationship of MYB96 with ABA and auxin, we investigated its expression patterns in response to exogenous ABA and IAA applications. Unlike in the plants treated with ABA, MYB96 transcripts were accumulated throughout the whole root system, including the vascular tissue in the IAA-treated plants. Detailed analysis revealed that MYB96 expression is initiated in the pericycle, the initiation site of lateral root formation. The expansion of MYB96 expression domain in the presence of auxin might be closely related with the promotive effects of auxin on the lateral root development.
When plants were treated with both ABA and IAA, the level of MYB96 transcript was lower than that observed in the IAA-treated roots, indicating that ABA inhibits the action of IAA on the pericycle cell division. Accordingly, less lateral root primordia were produced in the presence of IAA and ABA, which on its turn results in less cells expressing MYB96. It is therefore suggested that IAA and ABA act antagonistically and ABA is epistatic to auxin in certain lateral root developmental stages.
Linking with auxin homeostasis is a prominent point in the MYB96-mediated ABA signaling pathway. The MYB96 regulation of the GH3 genes is restricted to the roots, particularly in the lateral root primordia, suggesting that reduced lateral root number is caused by altered auxin metabolism. Auxin is a well-known regulator functioning throughout the whole lateral root growth and developmental process.13 In addition, auxin plays important roles in cell division and establishment of the lateral root meristem during the lateral root emergence stage.14,15 Recent studies have also suggested that extensive ABA-auxin interactions take places during the lateral root emergence stage.10 The promotive effects of auxin on the lateral root meristem activation might be inhibited by the repressive actions of ABA.15 Indeed, lateral root formation of the MYB96-overexpressing mutant is suppressed in the lateral root emergence stage, and this lateral root phenotype is not rescued by exogenous application of auxin. In this regard, the MYB96-mediated regulation of auxin metabolism to inhibit lateral root growth is an interesting example showing how ABA-auxin crosstalks occur during the lateral root development.
Web-based global gene expression analysis data suggest that MYB96 might also have a role in pathogenesis. When plants are treated with pathogen elicitor, such as bacterial flagellin peptide elicitor (flg22), oligogalacturonides (OG) and chitin, MYB96 expression is significantly induced. We recently found that endogenous level of salicylic acid (SA) and expression of SA biosynthetic genes are highly upregulated in the shoots of the MYB96-overexpressing mutant shoots (data unpublished). It is possible that MYB96 may also function as a molecular link that mediates ABA-SA crosstalks in the shoots (Fig. 1).
Previously published online: www.landesbioscience.com/journals/psb/article/9716