Banana MaNAC1 activates secondary cell wall cellulose biosynthesis to enhance chilling resistance in fruit

Abstract

SummaryChilling injury has a negative impact on the quantity and quality of crops, especially subtropical and tropical plants. The plant cell wall is not only the main source of biomass production, but also the first barrier to various stresses. Therefore, improving the understanding of the alterations in cell wall architecture is of great significance for both biomass production and stress adaptation. Herein, we demonstrated that the cell wall principal component cellulose accumulated during chilling stress, which was caused by the activation of MaCESA proteins. The sequence‐multiple comparisons show that a cold‐inducible NAC transcriptional factor MaNAC1, a homologue of Secondary Wall NAC transcription factors, has high sequence similarity with Arabidopsis SND3. An increase in cell wall thickness and cellulosic glucan content was observed in MaNAC1‐overexpressing Arabidopsis lines, indicating that MaNAC1 participates in cellulose biosynthesis. Over‐expression of MaNAC1 in Arabidopsis mutant snd3 restored the defective secondary growth of thinner cell walls and increased cellulosic glucan content. Furthermore, the activation of MaCESA7 and MaCESA6B cellulose biosynthesis genes can be directly induced by MaNAC1 through binding to SNBE motifs within their promoters, leading to enhanced cellulose content during low‐temperature stress. Ultimately, tomato fruit showed greater cold resistance in MaNAC1 overexpression lines with thickened cell walls and increased cellulosic glucan content. Our findings revealed that MaNAC1 performs a vital role as a positive modulator in modulating cell wall cellulose metabolism within banana fruit under chilling stress.

Function of the NAC1 Gene from <em>Fraxinus mandshurica</em> in Cold Resistance and Growth Promotion in Tobacco

“…In tomato fruit, the overexpression of MaNAC1 enhances cold resistance, leading to thicker cell walls and increased cellulose content. Similarly, in banana fruit, MaNAC1 acts as a positive regulator in governing cellulose metabolism within the cell wall [32]. Additionally, many NAC transcription factors are reportedly induced by cold stress and play pivotal roles in plant responses to such conditions [32].…”

“…Similarly, in banana fruit, MaNAC1 acts as a positive regulator in governing cellulose metabolism within the cell wall [32]. Additionally, many NAC transcription factors are reportedly induced by cold stress and play pivotal roles in plant responses to such conditions [32]. The identification of the NAC056 transcription factor, which enhances plant cold tolerance by upregulating genes in the CBF pathway and its association with the CBF1-NIA1 regulatory module, underscores the critical role of NAC056 in balancing plant growth and plant responses to cold stress [34].…”

Chilling stress response in tobacco seedlings: insights from transcriptome, proteome, and phosphoproteome analyses

“…They can activate the levels of expression of downstream genes, including COR (cold-regulated), LTI (low-temperature induced), and RD (responsive to dehydration) ( Zhu et al., 2007 ), which thereby improves the ability of plants to tolerate low temperatures. Other TFs, such as NAC1 ( Ma et al., 2013 ; Yin et al., 2024 ) and CAMTAs ( Kim et al., 2013 ), and kinase genes, including VaCPK20 ( Dubrovina et al., 2015 ), GsLRPK ( Yang et al., 2014 ), and the FERONIA receptor-like kinase gene MdMRLK2 ( Jing et al., 2023 ), are involved in this resistance to chilling stress. The development of omics technology enabled plant science researchers to reveal the complex mechanisms of the responses of plants to chilling stress.…”

MeGT2.6 increases cellulose synthesis and active gibberellin content to promote cell enlargement in cassava

“…Numerous reports had highlighted the role of transcription factors (TFs) in regulating cellulose synthesis and GA metabolism. In terms of cellulose synthesis, GhMYBL1 and MaNAC1 directly bind to the promoters of GhCesA4‐1 / 4‐2 / 8‐1 and MaCesA7 / 6B and then activate their expression to promote cellulose biosynthesis, thereby boosting SCW formation in cotton ( Gossypium hirsutum ) and banana ( Musa paradisiaca ; Wang et al., 2023; Yin et al., 2024). In addition, TFs can positively modulate the active GA content by regulating the transcription activities of GA20oxs .…”