A Comprehensive Framework for Plant Hormone Function: Nutrient Status Signaling and Cellular Coordination

1. Introduction

Plant hormones coordinate growth, development, and responses to environmental stimuli through complex signaling networks (Davies, 2010). Traditional approaches have focused on individual hormone functions, but emerging evidence suggests extensive crosstalk and interdependence among hormone pathways (Santner et al., 2009). This paper proposes a unifying framework where plant hormones primarily function as nutrient status signals, coordinating cellular responses based on resource availability.

The concept of hormones as resource indicators has precedent in animal physiology, where hormones like insulin signal nutrient abundance and coordinate anabolic processes (Saltiel & Kahn, 2001). Similarly, stress hormones like cortisol coordinate responses to resource scarcity (Sapolsky et al., 2000). We propose that plant hormones evolved analogous functions, with specific hormones indicating the abundance or scarcity of essential nutrient classes.

2. Theoretical Framework

2.1 Four-Class Nutrient Classification

We classify plant nutrients into four fundamental categories based on their origin and transport:

1. Gases: Oxygen and carbon dioxide, primarily obtained through photosynthesis and respiration
2. Minerals: Inorganic nutrients absorbed from soil through roots
3. Water: The universal solvent and transport medium
4. Carbohydrates: Energy-rich organic compounds produced through photosynthesis

This classification reflects the distinct physiological systems involved in nutrient acquisition and transport (Taiz et al., 2015).

2.2 Hormone-Nutrient Correspondence

We propose that eight major plant hormones function as paired abundance/deficiency signals for these four nutrient classes:

This pairing reflects observed physiological responses and provides a framework for understanding hormone interactions.

3. Detailed Hormone Analysis

3.1 Gas Signaling: Auxin and Ethylene

Auxin as Oxygen Abundance Signal

Auxin (indole-3-acetic acid, IAA) exhibits properties consistent with an oxygen abundance signal:

• Promotes root formation, increasing oxygen uptake capacity (Overvoorde et al., 2010)
• Levels peak during photosynthesis when oxygen production is maximal (Ljung et al., 2001)
• Induces cell elongation, consistent with aerobic growth (Hager, 2003)
• High concentrations can induce ethylene production, potentially through oxygen depletion (Swarup et al., 2007)

The transport of auxin from shoots to roots through phloem (Petrasek & Friml, 2009) supports its role in communicating photosynthetic oxygen status to root systems.

Ethylene as Oxygen Deficiency Signal

Ethylene production increases under anaerobic conditions and coordinates responses to oxygen limitation:

• Induces aerenchyma formation for gas transport during flooding (Drew et al., 2000)
• Promotes adventitious root formation to enhance gas exchange (Visser et al., 1996)
• Causes leaf abscission, reducing oxygen demand (Abeles et al., 1992)
• Inhibits root elongation while promoting radial expansion, optimizing gas exchange surface area (Jackson, 1985)

3.2 Mineral Signaling: Cytokinin and Strigolactones

Cytokinin as Mineral Abundance Signal

Cytokinins are synthesized primarily in roots and transported to shoots, consistent with their role as mineral status indicators:

• Promotes shoot growth when mineral nutrients are available (Kieber & Schaller, 2014)
• Stimulates cell division in conjunction with adequate mineral nutrition (Gordon et al., 2009)
• Delays senescence when mineral nutrition is sufficient (Gan & Amasino, 1995)
• Levels correlate with root uptake of nitrogen and other minerals (Takei et al., 2001)

Strigolactones as Mineral Deficiency Signal

Strigolactones coordinate responses to mineral limitation:

• Inhibit shoot branching, reducing mineral nutrient demand (Gomez-Roldan et al., 2008)
• Promote symbiotic associations with mycorrhizal fungi, enhancing mineral uptake (Akiyama et al., 2005)
• Increase root hair formation, expanding nutrient absorption surface (Kapulnik et al., 2011)
• Production increases under phosphorus deficiency (López-Ráez et al., 2008)

3.3 Water Signaling: Salicylic Acid and Abscisic Acid

Salicylic Acid as Water Abundance Signal

Salicylic acid (SA) exhibits properties consistent with water abundance signaling:

• Found abundantly in willow bark, trees typically growing near water sources (Vlot et al., 2009)
• Promotes stomatal opening under well-watered conditions (Khokon et al., 2011)
• Stimulates cell division when water is abundant (Rivas-San Vicente & Plasencia, 2011)
• Antagonizes ABA-mediated stress responses (Yasuda et al., 2008)

The apparent contradiction of SA closing stomata can be explained by its dual role in pathogen defense, where closure prevents pathogen entry regardless of water status (Melotto et al., 2006).

Abscisic Acid as Water Deficiency Signal

ABA is the established drought stress hormone:

• Closes stomata to reduce water loss (Cutler et al., 2010)
• Promotes root growth to enhance water uptake (Sharp & LeNoble, 2002)
• Induces synthesis of stress proteins and osmolytes (Yamaguchi-Shinozaki & Shinozaki, 2006)
• Inhibits growth processes that require high water availability (Finkelstein, 2013)

3.4 Carbohydrate Signaling: Jasmonic Acid and Gibberellin/Brassinosteroids

Jasmonic Acid as Carbohydrate Abundance Signal

Jasmonic acid (JA) coordinates responses to carbohydrate availability:

• Promotes storage root formation when carbohydrates are abundant (Wasternack & Hause, 2013)
• Stimulates defense compound synthesis using available carbon resources (Browse, 2009)
• Induces tuber formation, a carbohydrate storage process (Yoshihara et al., 1989)
• Levels peak during daylight when photosynthesis produces carbohydrates (Saniewski et al., 1998)

Gibberellin/Brassinosteroids as Carbohydrate Deficiency Signals

Gibberellins (GA) and brassinosteroids (BR) coordinate responses to carbohydrate limitation:

• Promote stem elongation ("bolting") to reach better light conditions (Hedden & Phillips, 2000)
• Mobilize stored starch during germination (Bethke et al., 1997)
• Inhibit root growth, reducing carbohydrate sinks (Achard et al., 2006)
• Stimulate α-amylase production for starch breakdown (Kaneko et al., 2002)

The classification of BR with GA reflects their synergistic effects on carbohydrate mobilization and growth promotion under resource limitation (Clouse, 2011).

4. Cellular Coordination Hypotheses

5. Alternative Organizational Schemes

5.1 Three-State Model

An alternative framework considers three physiological states:

This model acknowledges that excess nutrients can be as problematic as deficiency, requiring disposal mechanisms.

5.2 Environmental Context Model

A third organizational scheme incorporates environmental conditions:

This model emphasizes the importance of environmental context in hormone interpretation.

6. Implications and Predictions

6.1 Testable Predictions

1. Cell division assays: Tissue cultures should require all four abundance hormones for optimal division rates
2. Senescence induction: Simultaneous application of all four deficiency hormones should induce senescence more effectively than individual hormones
3. Nutrient depletion: Specific nutrient deficiencies should correlate with predicted hormone level changes
4. Hormone transport: Abundance hormones should be transported from nutrient-producing to nutrient-consuming tissues

6.2 Agricultural Applications

Understanding hormone-nutrient relationships could improve:

• Precision agriculture: Hormone profiles could indicate specific nutrient deficiencies
• Crop breeding: Selection for optimal hormone sensitivity could improve nutrient use efficiency
• Growth regulators: Targeted hormone applications could optimize resource allocation

6.3 Evolutionary Perspectives

This framework suggests that hormone signaling systems evolved to optimize resource allocation in the face of variable nutrient availability. The paired abundance/deficiency signals may have evolved from simpler regulatory systems, with increasing sophistication allowing more precise resource management.

7. Current Limitations and Future Directions

7.1 Methodological Challenges

• Hormone quantification: Current methods may not capture local hormone concentrations relevant to cellular decision-making
• Temporal dynamics: Hormone interactions occur on multiple timescales requiring improved temporal resolution
• Tissue specificity: Cell-type-specific hormone responses need better characterization

7.2 Knowledge Gaps

• Strigolactone functions: Recently discovered, requiring more research on mineral deficiency signaling
• Hormone interactions: Quantitative models of hormone crosstalk are lacking
• Environmental modulation: How environmental factors modify hormone interpretation needs clarification

7.3 Future Research Directions

1. Systems biology approaches: Integrating hormone, metabolite, and gene expression data
2. Single-cell analysis: Understanding hormone perception at cellular resolution
3. Evolutionary studies: Tracing hormone system evolution across plant lineages
4. Synthetic biology: Engineering simplified hormone systems to test hypotheses

8. Conclusion

The framework presented here offers a unifying perspective on plant hormone function, proposing that hormones primarily serve as nutrient status indicators coordinating cellular responses to resource availability. While speculative in nature, this framework generates testable predictions and provides new insights into hormone interactions.

The proposed four-hormone requirements for cell division and senescence represent significant departures from current thinking but are consistent with the logic of resource-dependent cellular processes. As our understanding of hormone crosstalk increases, such integrated perspectives may prove essential for understanding plant physiology.

This framework should be viewed as a working hypothesis to guide experimental design rather than established fact. Its value will ultimately be determined by its ability to generate new insights and improve our understanding of plant hormone biology.