PXY collaboration with other cambial regulators, ER, and MP, is essential for secondary growth

Abstract

Plants grow both in height, and in width. The process of radial expansion, known as secondary growth, generates the majority of the plant biomass through expansion of the vasculature, the plant’s water and nutrient conducting tissues. It is therefore imperative to understand how vascular growth is regulated. Secondary growth is facilitated by a collection of stem cells present in a meristem called the vascular cambium. The cambium gives rise to the water-conducting xylem and nutrient conducting phloem, on opposing sides via periclinal cell divisions. A receptor-like kinase PXY has been found to promote cell division in the cambium, and to control its ability to maintain distinct domains for xylem and phloem. Loss of PXY results in interspersal of these cell types.
PXY interacts with other components in regulating secondary growth. It was seen to genetically interact with another receptor-kinase and its family of genes, ER. However, comprehensive exploration of how these two genes and their families interact had not been determined. Similarly, PXY was shown to indirectly suppress the transcription factor MP in stem, but to be promoted by MP in root. Both components were also found to be localized in the same domain on the xylem side of the cambium, where the hormone auxin was shown to accumulate. Disruption of the auxin pattern or removal of PXY or MP results in defects in cambial function, but the basis of these interactions is not fully understood.
To address the questions surrounding PXY’s role in secondary growth, a bespoke method for measuring cell sizes and shapes from cross-sections of plants was developed. This method was employed to analyse PXY and ER families single and combinatorial mutants. Finally, a theoretical three-cell mathematical model was proposed examining PXY’s relationship with the transcription factor MP in controlling the accumulation of auxin in the cambium.
The results of these studies demonstrated that loss of PXY and ER families results in different consequences in stem and hypocotyl. In hypocotyl and in the absence of the PXY family, ER and its genetic paralogues promote hypocotyl radial growth in part, compensating for loss of PXY by promoting cell size increases, but this was not observed in stem. Moreover, loss of all of the PXY and ER genes results in complete suspension of secondary growth, suggesting that these two genetic pathways are required for the transition between primary and secondary growth. In the investigation of PXY’s relationship with the transcription factor MP in root, it was shown both numerically and analytically that a negative feedback loop between the two provides stability to the system, thus generating a more stable auxin gradient in the cambium. Thus, PXY interacts with both ER and MP to maintain vascular organisation and growth, and these interactions are essential for the induction of secondary expansion, as well as hormone patterning in order to promote cambial activity.