**5. A negative regulator of the NRP/NAC081/VPE signaling module confers tolerance to drought**

Plants can negatively modulate the NRP/DCD-mediated cell death response to suit the cellular balance during the stress conditions. Moreover, this modulation improves the cellular stableness and consequently increases the plant tolerance to stress conditions in an essential process that is required for plant acclimatization and development. The molecular chaperone BiP plays a crucial role as a negative regulator of NRP/DCD-mediated cell death response. BiP belongs to the HSP70 family, which is essential to protect the cells against environmental stresses and to restore the cell homeostasis [59].

The molecular chaperone BiP has a catalytic site at the amino-terminal region and a substrate-binding site at the carboxy-terminal region [60]. BiP is involved in the regulation of several processes in the endoplasmic reticulum, a critical organelle that is related to responses to abiotic and biotic stress in plants. In the ER, BiP acts as a sensor that responds to quantitative and qualitative changes in the ER by regulating the activity of ER stress transducers [61]. Furthermore, BiP coordinately regulates the cell death signaling, which connects the signals from osmotic and ER stress in a DCD/NRP-dependent manner [35, 36, 38].

BiP attenuates the NRP/DCD-mediated cell death signal propagation by the modulation of expression and activity of the pathway signaling components (**Figure 3**). BiP overexpression in soybean attenuates ER stress- and osmotic stress-mediated cell death, a phenotype that is linked to a delay in the induction of *GmNRP-A*, *GmNRP-B*, and *GmNAC81* under ER stress and osmotic stress [38]. Furthermore, enhanced accumulation of BiP in tobacco (*Nicotiana tabacum*) prevents the GmNRP- and GmNAC81-mediated induction of cell death-associated physiological and molecular markers, whereas silencing of endogenous BiP enhances the cell death response.

In addition to alleviating ER and osmotic stress-mediated cell death, the *BiP* overexpression in plants has also been shown to increase their tolerance to water deficits [62–64]. Enhanced accumulation of BiP in soybean, tobacco, and *Arabidopsis* promotes a delay in drought-induced senescence and wilting of leaves

**71**

*A Regulatory Circuit Integrating Stress-Induced with Natural Leaf Senescence*

**6. The stress-induced DCD/NRP-mediated cell death signaling** 

Leaf senescence is a natural process in plant development, which begins with a physiological transition between active photosynthetic leaves to degenerative and nutrient-recycling leaves. The classical age senescence-related symptom is the leaf yellowing caused by generalized chlorophyll loss. The age-induced senescence or naturally programmed leaf senescence, hereafter referred to as leaf senescence, occurs by plant aging and is precisely regulated by senescence-associated genes

Many SAGs are environmental- and stress-responsive genes, integrating a convergent regulatory cascade between natural plant development and stress-induced PCD [68]. At the molecular level, the onset of senescence is accompanied by a massive reprogramming of gene expression, probably controlled by senescenceassociated transcription factors. Among these, several NAC transcription factors have been associated with senescence regulation based on high-resolution temporal

In soybean, a transcriptomic analysis of senescing leaves reveals that 44% of the *GmNAC* genes were differentially expressed at the onset of leaf senescence. The most representative subfamilies of soybean senescence-associated *NAC* genes were the abiotic stress-induced SNAC-A (ATAF) subfamily, in which 90% of the members were differentially expressed during senescence, followed by the biotic stress-induced TERN subfamily, displaying 80% of the members differentially expressed during leaf senescence [43]. *GmNAC30* and *GmNAC81*, which belong to the SNAC-A and TERN subfamilies, respectively, are among the upregulated genes by leaf senescence [43, 59]. These results raise the hypotheses that the (i)

leading to a higher survival rate of overexpressing lines under water-deficit regimes [12, 38, 40, 63–64]. The BiP-mediated tolerance mechanism is not associated with conventional mechanisms of drought tolerance and avoidance, as the BiPoverexpressing lines do not display lower photosynthesis and transpiration rates than untransformed lines under drought, and the stomata closure and root growth are not stimulated under water deprivation. Furthermore, the *BiP*-overexpressing lines exhibit a lower induction of drought-related genes than WT under waterdeficit conditions, and the abscisic acid content in *BiP*-overexpressing plants is similar to untransformed lines, indicating that the BiP-mediated drought tolerance mechanism is independent on ABA [59, 64, 65]. Under drought conditions, the only variations observed in *BiP*-overexpressing lines are a delay in drought-induced leaf senescence and an attenuation in the drought induction of PCD-associated marker genes, which is associated with the protective function of BiP as a negative modulator of the DCD/NRP-mediated cell death response. A metabolomic approach was used to detect the metabolite profile of *BiP*-overexpressing lines under drought conditions [65]. Due to a higher osmolyte accumulation, mainly amino acids, the *BiP*-overexpressing plants can maintain the leaf turgidity upon drought stress, which is a phenotypic hallmark of the BiP-mediated tolerance to drought. The *BiP*overexpressing lines also display a higher accumulation of salicylic acid and upregulation of SA-responsive genes, which is associated with accelerated hypersensitive response triggered by *Pseudomonas syringae pv tomato* in soybean and tobacco [59, 65]. The SA signaling also activates the antioxidative metabolism, which may be linked to the BiP protective function to drought. Very importantly, the BiP modulation of the DCD/NRP-mediated cell death response does not impair the plant

*DOI: http://dx.doi.org/10.5772/intechopen.89498*

growth and development.

(SAGs) [66, 67].

expression profiles [69].

**positively regulates leaf senescence**

#### *A Regulatory Circuit Integrating Stress-Induced with Natural Leaf Senescence DOI: http://dx.doi.org/10.5772/intechopen.89498*

leading to a higher survival rate of overexpressing lines under water-deficit regimes [12, 38, 40, 63–64]. The BiP-mediated tolerance mechanism is not associated with conventional mechanisms of drought tolerance and avoidance, as the BiPoverexpressing lines do not display lower photosynthesis and transpiration rates than untransformed lines under drought, and the stomata closure and root growth are not stimulated under water deprivation. Furthermore, the *BiP*-overexpressing lines exhibit a lower induction of drought-related genes than WT under waterdeficit conditions, and the abscisic acid content in *BiP*-overexpressing plants is similar to untransformed lines, indicating that the BiP-mediated drought tolerance mechanism is independent on ABA [59, 64, 65]. Under drought conditions, the only variations observed in *BiP*-overexpressing lines are a delay in drought-induced leaf senescence and an attenuation in the drought induction of PCD-associated marker genes, which is associated with the protective function of BiP as a negative modulator of the DCD/NRP-mediated cell death response. A metabolomic approach was used to detect the metabolite profile of *BiP*-overexpressing lines under drought conditions [65]. Due to a higher osmolyte accumulation, mainly amino acids, the *BiP*-overexpressing plants can maintain the leaf turgidity upon drought stress, which is a phenotypic hallmark of the BiP-mediated tolerance to drought. The *BiP*overexpressing lines also display a higher accumulation of salicylic acid and upregulation of SA-responsive genes, which is associated with accelerated hypersensitive response triggered by *Pseudomonas syringae pv tomato* in soybean and tobacco [59, 65]. The SA signaling also activates the antioxidative metabolism, which may be linked to the BiP protective function to drought. Very importantly, the BiP modulation of the DCD/NRP-mediated cell death response does not impair the plant growth and development.
