Cross–talk between nitric oxide and Ca²⁺ in elevated CO₂-induced lateral root formation

Abstract

This study demonstrates a potential signaling pathway of CO₂-dependent stimulation in lateral root (LR) formation. Elevated CO₂ increases production of nitric oxide (NO), which subsequently stimulates the generation of cytosolic Ca²⁺ concentration by activating plasma membrane and/or intracellular Ca²⁺-permeable channels. Meanwhile, nitric oxide synthase (NOS), as one of the main NO source, requires Ca²⁺ and CaM as cofactors. This complex interaction involves transduction cascades of multiple signals that lead to the LR formation and development. Finally, this review highlights the the role of Ca²⁺ in the process that elevated CO₂ enhances the development of LRs through increased NO level.

The effect of elevated CO₂ on plants has occasioned a number of investigations in past several decades. It has been demonstrated that CO₂ enhancement has a profound impact on plant growth and development. Many studies have investigated plant responses to elevated CO₂ on the ecosystem, community, population, physiological and molecular scales.^1-4 Based previous studies, we reported that elevated CO₂ promoted the development of LRs of tomato and NO was a signaling molecule that controls these processes.⁵ Increased LRs could eliminate nutrient stress under elevated CO₂, which play an important role in nutrient acquisition.⁶

Lateral root formation can be divided into three key stages: (1) founder cell selection/initiation; (2) development and emergence of the LR primordia; (3) LR growth and orientation.⁷ Radially, only pericycle cells located adjacent to protoxylem poles can become founder cells. Founder cells differentiate and proliferate in a highly reproducible program to form LR primordia, and then further differentiate and elongate causing the LR to emerge through the epidermis. The rate of cell division and elongation in the meristem determines the growth rate of LRs. The direction of root growth is determined by various tropisms (i.e., phototropism, gravitropism, hydrotropism). Strong evidence indicates that LR development was regulated by several factors, such as low sulfate, low phosphate, nitrate–rich patch, iron deficiency and elevated CO₂.^5,8-11 Furthermore, auxin, ethylene, ABA and NO have all been implicated in the emergence and meristem activation.^12-15

NO has been proved as a multipurpose signaling messenger that accomplishes its biological functions through its action on multiple targets. The available data illustrate that NO can directly influence the activity of target proteins through nitrosylation and has the capacity to act as a Ca²⁺–mobilizing intracellular messenger. Several lines of evidence showed that a number of signal factors, such as NO, auxin, and cytosolic Ca²⁺ independently and/or synergistically induced root development and growth.^3,16-18 By increasing cytosolic Ca²⁺ concentration, NO modulates the activity of Ca²⁺–dependent protein kinases (CDPKs), mitogen–activated protein kinases (MAPKs), and Ca²⁺–sensitive channels, which might be involved in the signaling cascade related to auxin–mediated adventitious root formation and cell division.^16,19,20 Recent studies showed that elevated CO₂ increased auxin level and response,^2,3,21 and that production of NO was promoted in tomato roots under co–treatment with elevated CO₂ and iron deficiency.¹¹ Consequently, in this paper, we proposed that cross–talks between NO and Ca²⁺ involving in elevated CO₂ induced LR formation.

How does Elevated CO₂ Regulate LR Development?

Accumulating evidence strongly indicates that elevated CO₂ can accelerate plant growth and development by affecting cell division, elongation and differentiation within apical meristems.²² Calcium plays an important role in the regulation of many cellular processes in higher plants.²³ Likewise, NO could mediate the induction of cell cycle regulatory genes at the beginning of LR primordia formation in tomato.^15,24 Thus, changes in levels of NO and Ca²⁺ or its interaction may play an important role in regulating the development of LRs under elevated CO₂.

Our previous study reported that elevated CO₂ enhanced production of NO, which promoted development of LRs in tomato.⁵ Auxin and NO induced development of cucumber explants adventitious roots and rice LRs by increasing cytosolic Ca²⁺ concentration.^16,18 Further, it has been showed that elevated CO₂ significantly increased the uptake of calcium²⁵ and the concentration of cytosolic free calcium in guard cells.²⁶ These results imply that Ca²⁺ signaling cascade may involve in the process of elevated CO₂–induced LR formation.

On the other hand, we reported that it was the NOS rather than NR responsible to NO production under elevated CO₂.⁵ In animals, activities of the constitutive isoforms of mammalian NOSs (cNOSs) are strictly CaM/Ca²⁺–dependent.²⁷ Interestingly, plant NOS activity also requires Ca²⁺ and CaM as cofactors in several plant species.^28-31 In agreement with these findings, Ali et al. (2007) provided genetic evidence indicated that lipopolysaccharide–induced NO synthesis through NOS, is controlled by an upstream Ca²⁺ influx.³² Therefore, it is necessary to understand the interaction between NO and Ca²⁺ under the process that elevated CO₂ enhanced production of NO through NOS, which promoted development of LRs in tomato.

Wang H, Xiao W, Niu Y, Jin C, Chai R, Tang C, Zhang Y. Nitric oxide enhances development of lateral roots in tomato (Solanum lycopersicum L.) under elevated carbon dioxide. Planta. 2013;237:137–44. doi: 10.1007/s00425-012-1763-2.