The Novel Cucurbitaceae miRNA ClmiR86 Is Involved in Grafting-Enhanced Phosphate Utilization and Phosphate Starvation Tolerance in Watermelon.

Weifang Wu,Haoshun Zhao,Zhongyuan Hu,Qin Deng,Jinghua Yang,Pibiao Shi,Xiaoxiao Guan,Mingfang Zhang,Haiyang Yang,Rui Qi

doi:10.3390/plants10102133

Abstract

Watermelon (Citrullus lanatus) is a globally important Cucurbitaceae crop in which grafting is commonly used to improve stress tolerance and enhance nutrient utilization. However, the mechanism underlying grafting-enhanced nutrient assimilation remains unclear. Here, we demonstrate the possible involvement of a novel Cucurbitaceae miRNA, ClmiR86, in grafting-enhanced phosphate-starvation tolerance via CALCINEURIN B-LIKE INTERACTING PROTEIN KINASE 5 (ClCIPK5) suppression in watermelon. Transcript analyses revealed that the induction of ClmiR86 expression was correlated with the downregulation of ClCIPK5 in squash-grafted watermelon under phosphate starvation. In addition, the differential expression of ClmiR86 in various watermelon genotypes was consistent with their phosphate utilization efficiency. Furthermore, ClmiR86 overexpression in Arabidopsis enhanced root growth and phosphate uptake under phosphate starvation and promoted inflorescence elongation under normal conditions. These results suggest that the ClmiR86–ClCIPK5 axis is involved in phosphate starvation response as well as grafting-enhanced growth vigor and phosphate assimilation. The present study provides valuable insights for investigating long-distance signaling and nutrient utilization in plants.

Highlights

Grafting—the unification of different parts of two or more plants that grow together and form a new plant [1]—was found to improve resistance to various biotic and tolerance of various abiotic stresses [2,3,4,5]
Our previous study demonstrated that under phosphate deficiency, phosphate uptake and phosphate utilization efficiency (PUE) were significantly enhanced in squash-grafted watermelon compared with those
Phosphate starvation significantly decreased lateral root number in the wildtype seedlings but did not decrease this number in 35S::ClmiR86 seedlings (Figure 5A,C). Leaf growth in both wildtype and transgenic plants were dramatically inhibited by phosphate starvation, whereas ectopic ClmiR86 expression slightly rescued leaf area under stress (Figure 5D,E). These results suggest that ClmiR86 overexpression enhances root tolerance to phosphate starvation, and this effect may be associated with its regulation of CBL-interacting protein kinase (CIPK)

Summary

Introduction

Grafting—the unification of different parts of two or more plants that grow together and form a new plant [1]—was found to improve resistance to various biotic and tolerance of various abiotic stresses [2,3,4,5]. Since grafting has been commonly used in watermelon production to improve disease resistance, against the soil-borne. Squash grafting was found to increase nutrient uptake in watermelon [8,9,10,11,12]. Phosphorus is a crucial and limiting soil nutrient, and it is fundamental to plant growth, development, and propagation [13,14]. Because of precipitation and mineralization, the only form of soil phosphorus that can be assimilated by plants (inorganic phosphate) for vegetative growth and development is usually scarce [13,15,16]. Plants have evolved several adaptive responses, such as the expansion of the root system to accelerate soil exploration [17,18], improvement of high-affinity phosphate uptake capacity [19], and production and secretion of organic acids and phosphatases to solubilize and mobilize phosphate in the soil and apoplast [15,20]

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Results

Conclusion