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Keywords:

  • Cotton;
  • premature leaf senscence;
  • dominant gene;
  • resistance

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Results
  5. Discussion
  6. Materials and Methods
  7. Acknowledgements
  8. References

Cotton (Gossypium hirsutum L.) premature leaf senescence-resistant inbred XLZ33 and senescence-susceptible inbred lines XLZ13 were selected and crossed to produce F1, F1-reciprocal, F2 and BC1 generations for evaluation of leaf senescence process and inheritance. The results showed that leaf senescence processes for XLZ13 and XLZ33 were obviously different and leaf senescence traits could be distinguished between the two parents at particular periods of cotton growth. Inheritance anlysis for the cotton premature leaf senescence resistant trait further showed that the segregation in the F2 fit a 3:1 ratio inheritance pattern, with resistance being dominant. The backcross of F1 to the susceptible parent produced a 1:1 ratio, confirming that cotton premature leaf senescence resistant trait was from a single gene. The single dominant gene controlling cotton premature leaf senescence resistance in XLZ33 was named as cotton premature leaf senescence resistance 1, with the symbol cplsr1.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Results
  5. Discussion
  6. Materials and Methods
  7. Acknowledgements
  8. References

Plants leaf senescence, showing yellowing leaves, desiccation, and eventual abscission, is an important step in the plant life cycle and an integral part of plant growth and development (Kim et al. 2011). As the final stage of plant development, leaf senescence usually occurs in an age-dependent manner, and plays a vital role in nutrient recycling (Himelblau and Amasino 2001) and also acts as a determinant process for yield production in many crops, where crop yield is enhanced by longer growth periods (Thomas et al. 2003). In agricultural aspects, the occurrence of too early (premature senescence) or too late (late maturity) leaf senescence may have great influence on yield production for annual crops. Late maturity interferes with nutrient remobilization, thereby compromising photosynthetic activity in young leaves and reproductive success. By contrast, premature leaf senescence would stunt plant growth and reduce the plant's overall capacity to assimilate CO2 (Wingler et al. 2006).

Cotton (Gossypium hirsutum L.), the most important crop for plant fiber production, is a perennial, indeterminate plant that is cultured as an annual in agronomic production systems. However, premature leaf senescence in cotton has been occurring with increasing frequency in many cotton-growing countries, especially in China, and causes serious reductions in yield and quality of cotton (Dong et al. 2005). According to estimation, premature leaf senescence can cause about 15% yield losses of cotton in China annually, though yield loss was even higher than 20% and up to 40% in some years (Liu et al. 2011a).

In order to alleviate premature leaf senescence of cotton, quite a few efforts have been attempted. For example: early fruit removal for regulation of cotton's sink-source relationships to proper niches (Dong et al. 2009); relatively late-planted cotton with increased plant density for improvement of cotton growth and the uptake of potassium (Dong et al. 2006); potassium supplied for providing the nutritional requirement of cotton (Wright 1999; Zhu et al. 2010); application of external plant hormone may be a new development method for controlling of cotton premature leaf senescence as the characteristics of phytohormone changes during cotton senescence process are revealed (Dong et al. 2008). All these labor and economic cost methods can only alleviate premature senescence of cotton at a certain degree respectively, but cannot eliminate the yield loss caused by premature leaf senescence, especially when facing the situation such that most planted cotton varieties are susceptible to premature leaf senescence (Liu et al. 2011a). Thus, breeding and application of genetic resistance cotton varieties should be the major effective and economical strategies for controlling premature leaf senescence in cotton.

Our previous investigation showed different cotton varieties differ in resistance to premature leaf senescence (Liu et al. 2011a). Thus we wondered, is that resistance to premature leaf senescence for cotton an inheritance trait, and controlled by genes? In this study, the inheritance character of cotton for resistance to premature leaf senescence was investigated. The results showed that premature leaf senescence of cotton was controlled by a single dominant gene, named as cotton premature leaf senescence resistance 1, with the symbol of cplsr1. To our knowledge, this is the first case to report that the premature leaf senescence of cotton plant was controlled by a distinct dominant gene.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Results
  5. Discussion
  6. Materials and Methods
  7. Acknowledgements
  8. References

Differrence in leaf senescence processes between the two parents

The graph of leaf senescence index showed the leaf senescence processes for XLZ13 and XLZ33 were different (Figure 1). XLZ13 was shown to be susceptible to premature leaf senescence. Leaf senescence symptoms of XLZ13 began to occurin the second half of July, after which they entered a process of progressive development. Into late August, XLZ13 showed serious leaf senescence symptoms. On the 25th of August, the leaf senescence index for XLZ13 reached the value of 90.78%, and the peak symptoms of leaf senescence for XLZ13 occurred in the first half of September, while XLZ33 showed resistance to premature leaf senescence. Symptoms for leaf senescence of XLZ33 occurred 25–30 days late, in late August. On the 25th of August, the leaf senescence index for XLZ33 only reached a value of 18.37%. Thus, the obvious difference in leaf senescence trait could be distinguished between the two parents at this period (Figure 2). Then the leaf senescence process for XLZ33 eventually developed through the first half of September, til to the second half of September. The leaf senescence processes for crossed F1 and F1 reciprocal plants, similarly to the resistance parent of XLZ33, showed the character of resistance to premature leaf senescence (Figures 1, 2).

image

Figure 1. Leaf senescence process.  ▪ Premature leaf senescence-susceptible inbred line XLZ13; □ Premature leaf senescence-resistant inbred line XLZ33; ▴ F1 (XLZ33 × XLZ13); △ F1 reciprocal (XLZ13 × XLZ33).

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image

Figure 2. Premature leaf senescence trait distinguished between the parental and F1 generations.  (A) Senescence-resistant inbred line XLZ33.  (B) Senescence-susceptible inbred line XLZ13.  (C) F1 (XLZ33 × XLZ13).  (D) F1 reciprocal (XLZ13 × XLZ33).  (E) Senescence-resistant inbred line XLZ33.  (F) Senescence-susceptible inbred line XLZ13.  (G) F1 (XLZ33 × XLZ13).  (H) F1 reciprocal (XLZ13 × XLZ33).  (A), (B), (C), and (D) were photographed on 25th of August; (E), (F), (G), and (H) were photographed on 5th of September.

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The cotton leaves’ senescence also showed an obvious development pattern. At the initial stage, leaves began to appear yellow, and exhibit chlorosis from plant bottom upwards. Leaves photosythesis function was declined or lost. To late stage, senescence leaves turned to desiccation, and eventual abscission, which led to serious petal or bud falling symptoms and often showing a phenomenon such that there were no leaves on the fruit branches locating immature cotton bolls (Figure 3). This kind of immature cotton boll cannot mature further. Accompanying leaf senescence, cotton leaves were getting more susceptible to attack by the cotton leaf spot disease pathogen Alternaria. With the infection of the leaf disease pathogens and expansion of spot lesions, the cotton leaves entered into an accelerated senescence process (Figure 3 arrow indication).

image

Figure 3. The development processes of cotton leaf senescence.  (A) Healthy leaf.  (B) Initial stage of leaf senescence.  (C-D) Developing stage of leaf senescence.  (E) Desiccation leaf.  (F) Abscission leaves.  (G) Petal or bud falling cotton plant.  (H) Immaturity cotton bolls without leaves.  White arrows indicate leaf spot lesions caused by cotton leaf spot disease pathogen Alternaria spp.

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Dominant characteristic for cotton leaf senescence and segregation in F2 and BC1 generations

The results showed that the cotton premature leaf senescence resistance was a dominant characteristic. Almost all F1 and F1-reciprocal plants were resistant to premature leaf senescence, and showed similar leaf senescence symptoms and processes as the resistant parent of XLZ33. The resistance character was segregated in F2 and BC1-P2 generations (Table 1). The F2 segregated in a 3:1 resistance/susceptible ratio (Table 2). The BC1-P1 plants, the backcrossed generation to the resistant parent, were all resistant, whereas the BC1-P2 plants, the backcrossed generation to the susceptible parents, segregated in a 1:1 ratio (Table 2). Thus, the trait for cotton resistance to premature leaf senescence was quite possibly controlled by a single dominant gene. This gene is named as cotton premature leaf senescence resistance 1, with the symbol of cplsr1.

Table 1.  Rating for resistance to leaf senescence in crosses of XLZ33 with XLZ13
Parents or crossesNo. of plantsSenescence rating (No. of plants in category)Average resistance ratingTotal variance
01234
  1. Senescence rating was 0 to 4 (0, no senescence symptoms, whole plant leaves are green and healthy; 1, senescence leaves with yellowing symptom accounting for no more than 25% of the whole plant leaves; 2, senescence leaves with yellowing symptom accounting for 25%–50% of the whole plant leaves; 3, senescence leaves with yellowing symptom accounting for 50%–75% of the whole plant leaves; 4, more than 75% senescence leaves showing extensive yellowing, desiccation, and abscission).

Resistant P1 (XLZ33) 857663000.1430.196
Susceptible P2 (XLZ13) 85 00228 55 3.6310.284
F1 (XLZ33 × XLZ13)1047510 13 420.5440.976
F1-reciprocal (XLZ13 × XLZ33)1048879000.2430.362
F2 (XLZ33 × XLZ13)14787920 17 14 1.0682.064
F2 (XLZ13 × XLZ33)133907811 17 0.9392.241
BC1-P1 (XLZ33 × XLZ13) × XLZ3313011210 6200.2170.359
BC1-P2 (XLZ33 × XLZ13) × XLZ1316565519 47 28 1.9102.511
Table 2.  Inheritance of resistance to premature leaf senescence in crosses of cotton XLZ33 with XLZ13
Parents or crossesNo. of plantsResistant plantsSusceptible plantsExpected ratio X 2 (correction) P value
  1. Segregation ratios were compared to the expected ratios with Chi-square test and corrected by Yates’ correction for continuity.

Resistant P1 (XLZ33) 85 85 01:0  
Susceptible P2 (XLZ13) 85  2830:1  
F1 (XLZ33 × XLZ13)104 98 61:0  
F1-reciprocal (XLZ13 × XLZ33)104104 01:0  
F2 (XLZ33 × XLZ13)133105283:10.900.34
F2 (XLZ13 × XLZ33)147116313:11.000.32
BC1-P1 (XLZ33 × XLZ13) × XLZ33130128 21:0  
BC1-P2 (XLZ33 × XLZ13) × XLZ13165 89761:10.870.35

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Results
  5. Discussion
  6. Materials and Methods
  7. Acknowledgements
  8. References

As the final stage of plant development, leaf senescence has a crucial impact on yield production for crops. On one hand, premature leaf senescence curtails carbon assimilation, stunts plant growth and reduces yield (Thomas and Howarth 2000). On the other hand, leaf senescence is a positive, altruistic and complex regulated process, in which the released nutrients are transferred to developing fruits and seeds, and contributes to the fitness of whole plants by ensuring optimal production of offspring and better survival of plants in their temporal and spatial niches (Gan 2007; Lim et al. 2007).

Leaf senescence is basically governed by the developmental age, and induced by complex endogenous signals or initiated by a number of exogenous environmental stresses, including age, developmental cues, plant growth regulators, light and temperature stress, dehydration, nutrient deficiency, and pathogen infection (Zhou et al. 2009; Zhao et al. 2012). In agricultural production systems, premature leaf senescence often heavily influences crop yield production, but it is difficult to distinguish the key factor for the cause of leaf senescence and carry out proper approaches for alleviating premature leaf senescence. The outstanding example is cotton planting in China, where cotton premature leaf senescence has been occurring seriously and with increasing frequency for ten years. Thus, efforts focusing on physiological regulation (Dong et al. 2009, 2006), nutritional supplement (Wright 1999; Zhu et al. 2010) and external plant hormone application (Dong et al. 2008) have been attempted to prevent premature leaf senescence in cotton. These efforts have brought some positive methods to alleviate premature senescence to a certain degree, but still cannot eliminate the greatly yield loss caused by premature leaf senescence.

It is expected to develop and apply novel and effective approaches for controlling premature leaf senescence in crops depending on further revealing physiological and genetic mechanisms of plant leaf senescence.

Presently, investigations focused on revealing physiological and genetic mechanisms for plant leaf senescence processes were mainly performed on the model plant, Arabidopsis thaliana, which provided some direct evidence that plant hormones played key roles in responses to plant leaf senescence. Plant leaf senescence is accelerated by the hormones ethylene, abscisic acid (ABA), and jasmonic acid (JA) and delayed by cytokinin and auxin. Ethylene-insensitive mutants such as ethylene resistant 1 (etr1) and ethylene-insensitive 2 (ein2) display delayed leaf senescence (Bleecker et al. 1988; Chao et al. 1997). ABA accelerates senescence (Weaver et al. 1998). Exogenous methyl jasmonic acid (MeJA) has been reported to accelerate leaf senescence, and the JA-insensitive mutant, coronatine insensitive 1 (coi1) fails to display JA-dependent senescence (He et al. 2002). Cytokinins have been shown to play key roles in the delay of leaf senescence in tobacco (Rivero et al. 2007), petunia (Chang 2003), cassava (Zhang et al. 2010), and lettuce (Gan and Amasino 1995). An over-expressing YUCCA6 protein, a flavin monooxygenase protein controlling the rate-limiting step in de novo auxin biosynthesis in Arabidopsis thaliana, has been shown to contain elevated free indole-3-acetic acid levels and displayed dramatic leaf longevity (Kim et al. 2011).

Recently, with the development of various genetic and profiling approaches and methods, identification and characterization for genes that showed enhanced or reduced expression during leaf senescence with genome-wide microarray analysis has also been extensively investigated with the model plant Arabidopsis thaliana. A large amount of plant leaf senescence-associated genes (SAGs) involved in plant leaf senescence have been identified (Liu et al. 2011b; Jiang et al. 2011). Among them, more than 200 transcription factors are involved in the regulation of leaf senescence, and several transcription factors, including NAC (Yang et al. 2011), MYB (Zhang et al. 2011), RAV1 (Woo et al. 2010), and CBF2 (Sharabi-Schwager et al. 2010), have been demonstrated to play important roles in the regulation of leaf senescence, indicating that leaf senescence is governed by complex transcriptional regulatory networks. Furthermore, signaling pathways of MKK9-MPK3/MPK6 cascades involved in ethylene signaling have been demonstrated to play an important role in the regulation of leaf senescence (Zhou et al. 2009). A recent high-resolution temporal profiling of transcripts reveals a distinct chronology of metabolic processes and signaling pathways during leaf senescence (Breeze et al. 2011). These advances which were mainly performed with reverse genetics approaches on the model plant Arabidopsis thaliana have enhanced our understanding that the nature of plant leaf senescence may actually be controlled by certain genes. These results also provide a quantifiable and global picture of the leaf senescence process at the gene expression level, and these data may be further utilized for connection of metabolic processes, signaling pathways, and specific TF activity involved in the leaf senescence process, which would underpin the development of network models to elucidate the process of senescence.

In contrast to the model plant Arabidopsis thaliana, knowledge about the genetic and molecular basis for the leaf senescence process of crop plants is still poorly understood considering that leaf senescence for most crops is accompanied by the development of reproductive structures, which unlike in Arabidopsis leaf senescence. Thus, the findings in Arabidopsis might not reveal some of the mechanisms involved in leaf senescence of crop plants. At present, investigations on inheritance concerning leaf senescence for most crops are still poor, let alone revealing the leaf senescence mechanisms involved in crop plants.

When the significant difference in resistance to premature leaf senescence for different cotton varieties was revealed (Liu et al. 2011a), the investigation of the inheritance characteristics for cotton leaf senescence were performed on the selected premature leaf senescence resistant inbred XLZ33 and susceptible inbred lines XLZ13. The results clearly confirmed the cotton premature leaf senescence resistance of XLZ33 was controlled by a single completely dominant gene, named cotton premature leaf senescence resistance 1, with the symbol of cplsr1. To our knowledge, cplsr1 is the first identified gene for controlling premature leaf senescence in cotton plant. The result that cotton premature leaf senescence is controlled by a single completely dominant gene was in agreement with previous genetic analysis for leaf senescence trait in maize (Ceppi et al. 1987).

The identified cotton premature leaf senescence resistance gene cplsr1 can be used either routinely for introducing leaf senescence resistance into new cotton cultivars and eliminating yield loss caused by cotton premature leaf senescence or used to further reveal the molecular basis of the cotton leaf senescence process.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Results
  5. Discussion
  6. Materials and Methods
  7. Acknowledgements
  8. References

Plant materials and field management

The parent genetic plant materials used in this study were premature leaf senescence resistant inbred population seeds of XLZ33 and susceptible inbred population seeds of XLZ13, provided by Li Jiasheng researcher (Institute of Agricultural Sciences, Kuitun, Xinjiang). Leaf senescence characters for these two parents were further confirmed by our previous study (Liu et al. 2011). XLZ33 (P1) was crossed with XLZ13 (P2) to produce F1 (XLZ33 × XLZ13), F1 reciprocal (XLZ13 × XLZ33), F2, BC1-P1[(XLZ33 × XLZ13) × XLZ33] and BC1-P2[(XLZ33 × XLZ13) × XLZ13] generations.

Field experiments in 2009, 2010 and 2011 were performed at the LangFang Experimental Station of IPPCAAS, CAAS (39° 30′ N, 116° 36′ E), located in LangFang city, Hebei province, China. Cotton was sown under the plastic mulching production system in last week of April, and field managements were performed mainly according to previously described (Dong et al. 2006) with targeted plant density of 4–5 plants/m2. Other management practices were conducted according to local agronomic recommendations unless otherwise indicated. Experiments in 2009 focused on distinguishing the different characters of leaf senescence traits among two parents and F1 generations. In experiments in 2010 and 2011, leaf senescence grades were evaluated for single cotton plant of all tested plant materials, including two parents, F1, F2 and BC1 generations. Results of the two years analyzed had similar responses so data from the two years were combined and analyzed together.

Leaf senescence evaluation

Symptoms of leaf senescence on cotton plants were rated at ten-day intervals from 25th July to 15th September 6 times as described previously (Liu et al. 2011a). The rating was on a scale of 0–4 (0 = no symptoms, whole plant leaves are green and healthy; 1 = senescent leaves with yellowing symptoms accounting for no more than 25% of the whole plant leaves; 2 = senescent leaves with yellowing symptoms accounting for 25%–50% of the whole plant leaves; 3 = senescent leaves with yellowing symptom accounting for 50%–75% of the whole plant leaves; 4 = more than 75% senescent leaves shown to have extensive yellowing, desiccation, and abscission. The cotton leaf senescence index was calculated according to following formula:

Leaf senescence index = (∑ leaf senescence scores × number of senescence plants for each scores) / (total number of investigated plants × the highest grade senescence score) × 100.

Inheritance analysis

The investigation data on 25th August were selected for inheritance analysis. At this time, the susceptible parent of XLZ13 showed serious leaf senescence symptoms, while the resistance parents of XLZ33 had just begun to exhibit leaf senescence symptoms, the two parents showed significant differences in leaf senescence symptoms. Segregation ratios for F2 and BC1-P2 generations were compared to the expected ratios with Chi-square test and corrected by Yates’ correction for continuity using the following formula:

  • image

(Co-Editor: Hai-Chun Jing)

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Results
  5. Discussion
  6. Materials and Methods
  7. Acknowledgements
  8. References

We are grateful to Researcher Li Jiasheng for kindly providing XLZ13 and XLZ33 cotton seeds. This work was supported by the Xinjiang Production and Construction Corps Fund Project (2009JC004; 2011AB009), and the National Science and Technology Supported Project (2012BAD19B05).

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  1. Top of page
  2. Abstract
  3. Introduction
  4. Results
  5. Discussion
  6. Materials and Methods
  7. Acknowledgements
  8. References
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